PGRMC1 contributes to doxorubicin-induced chemoresistance in MES-SA uterine sarcoma

Cellular and Molecular Life Sciences

Volumn 72, Issue 12, 2015, Pages 2395-2409

  Lin, Szu Ting ^a   May, Eugenie Wong Soon ^a   Chang, Jo Fan ^a   Hu, Ren Yu ^a   Wang, Lily Hui Ching ^a   Chan, Hong Lin ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

Andriamycin; Drug resistant; Metastasis; Programed cell death; Uterine cancer

Indexed keywords

DOXORUBICIN; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR MEMBRANE COMPONENT 1; UNCLASSIFIED DRUG; VERAPAMIL; ANTINEOPLASTIC ANTIBIOTIC; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN; PGRMC1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG MECHANISM; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IC50; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UTERUS SARCOMA; ANTAGONISTS AND INHIBITORS; APOPTOSIS; CELL ADHESION; CELL CYCLE; CELL MOTION; DRUG RESISTANCE; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PATHOLOGY; SARCOMA; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; UTERINE NEOPLASMS; WESTERN BLOTTING;

ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BLOTTING, WESTERN; CELL ADHESION; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MEMBRANE PROTEINS; P-GLYCOPROTEIN; RECEPTORS, PROGESTERONE; RNA, SMALL INTERFERING; SARCOMA; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; UTERINE NEOPLASMS;

EID: 84929707805     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1831-9     Document Type: Article

References (43)

1. Gao Y, Meng H, Zhang Y, Jiao T, Hui N (2014) Retrospective analysis of 80 cases with uterine carcinosarcoma, leiomyosarcoma and endometrial stromal sarcoma in China, 1988-2007. Int J Clin Exp Pathol 7(4):1616-1624
2. D'Angelo E, Prat J (2010) Uterine sarcomas: a review. Gynecol Oncol 116(1):131-139. doi: 10.1016/j.ygyno.2009.09.023
3. Yoon KA, Ku JL, Yang JO, Park JG (2003) Telomerase activity, expression of Bcl-2 and cell cycle regulation in doxorubicin resistant gastric carcinoma cell lines. Int J Mol Med 11(3):343-348
4. Vatsyayan R, Chaudhary P, Lelsani PC, Singhal P, Awasthi YC, Awasthi S, Singhal SS (2009) Role of RLIP76 in doxorubicin resistance in lung cancer. Int J Oncol 34(6):1505-1511
5. Wang J, Qu H, Jin L, Zeng W, Qin L, Zhang F, Wei X, Lu W, Zhang C, Liang W (2011) Pegylated phosphotidylethanolamine inhibiting P-glycoprotein expression and enhancing retention of doxorubicin in MCF7/ADR cells. J Pharm Sci 100(6):2267-2277. doi: 10.1002/jps.22461
6. Deffie AM, Batra JK, Goldenberg GJ (1989) Direct correlation between DNA topoisomerase II activity and cytotoxicity in adriamycin-sensitive and -resistant P388 leukemia cell lines. Cancer Res 49(1):58-62
7. Yamamoto M, Maehara Y, Sakaguchi Y, Kusumoto T, Baba H, Sugimachi K (1997) The quinolinone derivative vesnarinone potentiates the cytotoxicity of doxorubicin in HL-60 leukemia cells. Int J Oncol 10(1):53-57
8. Beaumont PO, Moore MJ, Ahmad K, Payne MM, Lee C, Riddick DS (1998) Role of glutathione S-transferases in the resistance of human colon cancer cell lines to doxorubicin. Cancer Res 58(5):947-955
9. Morrow CS, Cowan KH (1990) Multidrug resistance associated with altered topoisomerase II activity-topoisomerases II as targets for rational drug design. J Natl Cancer Inst 82(8):638-639
10. Lin ST, Chou HC, Chang SJ, Chen YW, Lyu PC, Wang WC, Chang MD, Chan HL (2012) Proteomic analysis of proteins responsible for the development of doxorubicin resistance in human uterine cancer cells. J Proteomics 75(18):5822-5847. doi: 10.1016/j.jprot.2012.07.047
11. Mifsud W, Bateman A (2002) Membrane-bound progesterone receptors contain a cytochrome b5-like ligand-binding domain. Genome Biology 3:research0068-research0068.5. doi: 10.1186/gb-2002-3-12-research0068
12. Cahill MA (2007) Progesterone receptor membrane component 1: an integrative review. J Steroid Biochem Mol Biol 105(1-5):16-36. doi: 10.1016/j.jsbmb.2007.02.002
13. Hughes AL, Powell DW, Bard M, Eckstein J, Barbuch R, Link AJ, Espenshade PJ (2007) Dap1/PGRMC1 binds and regulates cytochrome P450 enzymes. Cell Metab 5(2):143-149. doi: 10.1016/j.cmet.2006.12.009
14. Crudden G, Loesel R, Craven RJ (2005) Overexpression of the cytochrome p450 activator hpr6 (heme-1 domain protein/human progesterone receptor) in tumors. Tumour Biol 26(3):142-146. doi: 10.1159/000086485
15. Difilippantonio S, Chen Y, Pietas A, Schluns K, Pacyna-Gengelbach M, Deutschmann N, Padilla-Nash HM, Ried T, Petersen I (2003) Gene expression profiles in human non-small and small-cell lung cancers. Eur J Cancer 39(13):1936-1947
16. Peluso JJ, Liu X, Saunders MM, Claffey KP, Phoenix K (2008) Regulation of ovarian cancer cell viability and sensitivity to cisplatin by progesterone receptor membrane component-1. J Clin Endocrinol Metab 93(5):1592-1599. doi: 10.1210/jc.2007-2771
17. Ahmed IS, Rohe HJ, Twist KE, Mattingly MN, Craven RJ (2010) Progesterone receptor membrane component 1 (Pgrmc1): a heme-1 domain protein that promotes tumorigenesis and is inhibited by a small molecule. J Pharmacol Exp Ther 333(2):564-573. doi: 10.1124/jpet.109.164210
18. Peluso JJ, Gawkowska A, Liu X, Shioda T, Pru JK (2009) Progesterone receptor membrane component-1 regulates the development and Cisplatin sensitivity of human ovarian tumors in athymic nude mice. Endocrinology 150(11):4846-4854. doi: 10.1210/en.2009-0730
19. Neubauer H, Clare SE, Wozny W, Schwall GP, Poznanovic S, Stegmann W, Vogel U, Sotlar K, Wallwiener D, Kurek R, Fehm T, Cahill MA (2008) Breast cancer proteomics reveals correlation between estrogen receptor status and differential phosphorylation of PGRMC1. Breast Cancer Res 10(5):R85. doi: 10.1186/bcr2155
20. Hand RA, Craven RJ (2003) Hpr6.6 protein mediates cell death from oxidative damage in MCF-7 human breast cancer cells. J Cell Biochem 90(3):534-547. doi: 10.1002/jcb.10648
21. Zhu X, Han Y, Fang Z, Wu W, Ji M, Teng F, Zhu W, Yang X, Jia X, Zhang C (2013) Progesterone protects ovarian cancer cells from cisplatin-induced inhibitory effects through progesterone receptor membrane component 1/2 as well as AKT signaling. Oncol Rep 30(5):2488-2494. doi: 10.3892/or.2013.2680
22. Hand RA, Jia N, Bard M, Craven RJ (2003) Saccharomyces cerevisiae Dap1p, a novel DNA damage response protein related to the mammalian membrane-associated progesterone receptor. Eukaryot Cell 2(2):306-317
23. Li JM, Wang YY, Zhao MX, Tan CP, Li YQ, Le XY, Ji LN, Mao ZW (2012) Multifunctional QD-based co-delivery of siRNA and doxorubicin to HeLa cells for reversal of multidrug resistance and real-time tracking. Biomaterials 33(9):2780-2790. doi: 10.1016/j.biomaterials.2011.12.035
24. Singh A, Settleman J (2010) EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 29(34):4741-4751. doi: 10.1038/onc.2010.215
25. Echizen H, Eichelbaum M (1986) Clinical pharmacokinetics of verapamil, nifedipine and diltiazem. Clin Pharmacokinet 11(6):425-449. doi: 10.2165/00003088-198611060-00002
26. Peluso JJ, Pappalardo A, Losel R, Wehling M (2006) Progesterone membrane receptor component 1 expression in the immature rat ovary and its role in mediating progesterone's antiapoptotic action. Endocrinology 147(6):3133-3140. doi: 10.1210/en.2006-0114
27. Kang YJ, Zhou Z-X, Wang G-W, Buridi A, Klein JB (2000) Suppression by metallothionein of doxorubicin-induced cardiomyocyte apoptosis through Inhibition of p38 mitogen-activated Protein Kinases. J Biol Chem 275(18):13690-13698. doi: 10.1074/jbc.275.18.13690
28. Ohtsuka T, Buchsbaum D, Oliver P, Makhija S, Kimberly R, Zhou T (2003) Synergistic induction of tumor cell apoptosis by death receptor antibody and chemotherapy agent through JNK/p38 and mitochondrial death pathway. Oncogene 22(13):2034-2044. doi: 10.1038/sj.onc.1206290
29. Strauss R, Hamerlik P, Lieber A, Bartek J (2012) Regulation of stem cell plasticity: mechanisms and relevance to tissue biology and cancer. Mol Ther J Am Soc Gene Ther 20(5):887-897. doi: 10.1038/mt.2012.2
30. Neganova I, Zhang X, Atkinson S, Lako M (2009) Expression and functional analysis of G1 to S regulatory components reveals an important role for CDK2 in cell cycle regulation in human embryonic stem cells. Oncogene 28(1):20-30. doi: 10.1038/onc.2008.358
31. Ben-Abdallah M, Sturny-Leclere A, Ave P, Louise A, Moyrand F, Weih F, Janbon G, Memet S (2012) Fungal-induced cell cycle impairment, chromosome instability and apoptosis via differential activation of NF-kappaB. PLoS Pathog 8(3):e1002555. doi: 10.1371/journal.ppat.1002555
32. Costa RH (2005) FoxM1 dances with mitosis. Nat Cell Biol 7(2):108-110. doi: 10.1038/ncb0205-108
33. Carr JR, Park HJ, Wang Z, Kiefer MM, Raychaudhuri P (2010) FoxM1 mediates resistance to herceptin and paclitaxel. Cancer Res 70(12):5054-5063. doi: 10.1158/0008-5472.CAN-10-0545
34. Khonkarn R, Mankhetkorn S, Talelli M, Hennink WE, Okonogi S (2012) Cytostatic effect of xanthone-loaded mPEG-b-p(HPMAm-Lac2) micelles towards doxorubicin sensitive and resistant cancer cells. Coll Surf B 94:266-273. doi: 10.1016/j.colsurfb.2012.02.002
35. Chen H, Qin Y, Zhang Q, Jiang W, Tang L, Liu J, He Q (2011) Lactoferrin modified doxorubicin-loaded procationic liposomes for the treatment of gliomas. Eur J Pharm Sci 44(1-2):164-173. doi: 10.1016/j.ejps.2011.07.007
36. Thomson S, Buck E, Petti F, Griffin G, Brown E, Ramnarine N, Iwata KK, Gibson N, Haley JD (2005) Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res 65(20):9455-9462. doi: 10.1158/0008-5472.CAN-05-1058
37. Ahmed IS, Rohe HJ, Twist KE, Craven RJ (2010) Pgrmc1 (progesterone receptor membrane component 1) associates with epidermal growth factor receptor and regulates erlotinib sensitivity. J Biol Chem 285(32):24775-24782. doi: 10.1074/jbc.M110.134585
38. Zavadil J, Bottinger EP (2005) TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24(37):5764-5774. doi: 10.1038/sj.onc.1208927
39. Kang Y, Massague J (2004) Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118(3):277-279. doi: 10.1016/j.cell.2004.07.011
40. Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG (2013) Cancer drug resistance: an evolving paradigm. Nat Rev Cancer 13(10):714-726. doi: 10.1038/nrc3599
41. Quan P, Moinfar F, Kufferath I, Absenger M, Kueznik T, Denk H, Zatloukal K, Haybaeck J (2014) Effects of targeting endometrial stromal sarcoma cells via histone deacetylase and PI3K/AKT/mTOR signaling. Anticancer Res 34(6):2883-2897
42. Thomas H, Coley HM (2003) Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting p-glycoprotein. Cancer Control 10(2):159-165
43. Yusa K, Tsuruo T (1989) Reversal mechanism of multidrug resistance by verapamil: direct binding of verapamil to P-glycoprotein on specific sites and transport of verapamil outward across the plasma membrane of K562/ADM cells. Cancer Res 49(18):5002-5006