Bcl-xL mediates therapeutic resistance of a mesenchymal breast cancer cell subpopulation

Oncotarget

Volumn 5, Issue 23, 2014, Pages 11778-11791

  Keitel, Ulrike ^a   Scheel, Andreas ^b   Thomale, Jürgen ^c   Halpape, Rovena ^d   Kaulfuß, Silke ^d   Scheel, Christina ^e,f   Dobbelstein, Matthias ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b Institute of Pathology Nordhessen   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^e WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^f Institute for Stem Cell Research Helmholz Center Munich   (Germany)

Author keywords

Apoptosis; Bcl xL; BH3 mimetic; Chemo resistance; Epithelial mesenchymal transition

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BIM PROTEIN; CARBOPLATIN; CISPLATIN; DOXORUBICIN; GOSSYPOL; PROTEIN BCL XL; PUMA PROTEIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; ZINOSTATIN; BCL2L1 PROTEIN, HUMAN; PROTEIN BCL X; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CARCINOMA; BREAST EPITHELIUM CELL; CANCER CELL; CANCER INHIBITION; CELL CULTURE; CELL INVASION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; DRUG RESISTANCE; DRUG SENSITIVITY; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INTRADUCTAL CARCINOMA; MESENCHYME CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR XENOGRAFT; ANIMAL; BIOSYNTHESIS; BREAST TUMOR; DNA MICROARRAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; BCL-X PROTEIN; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HETEROGRAFTS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTOME;

EID: 84920019403     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2634     Document Type: Article

References (39)

1. Boyer B, Tucker GC, Valles AM, Franke WW, Thiery JP. Rearrangements of desmosomal and cytoskeletal proteins during the transition from epithelial to fibroblastoid organization in cultured rat bladder carcinoma cells. The Journal of cell biology. 1989; 109:1495-1509.
2. Oft M, Peli J, Rudaz C, Schwarz H, Beug H, Reichmann E. TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes & development. 1996; 10:2462-2477.
3. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA.The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008; 133:704-715.
4. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature reviews Cancer. 2009; 9:265-273.
5. Tryndyak VP, Beland FA, Pogribny IP. E-cadherin transcriptional down-regulation by epigenetic and microRNA-200 family alterations is related to mesenchymal and drug-resistant phenotypes in human breast cancer cells. International journal of cancer Journal international du cancer. 2010; 126:2575-2583.
6. Asiedu MK, Ingle JN, Behrens MD, Radisky DC, Knutson KL. TGFbeta/TNF(alpha)-mediated epithelialmesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer research. 2011; 71:4707-4719.
7. Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R, Gray MJ, Cheng H, Hoff PM, Ellis LM. Chronic oxaliplatin resistance induces epithelialto-mesenchymal transition in colorectal cancer cell lines. Clinical cancer research: an official journal of the American Association for Cancer Research. 2006; 12:4147-4153.
8. Kajiyama H, Shibata K, Terauchi M, Yamashita M, Ino K, Nawa A, Kikkawa F. Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. International journal of oncology. 2007; 31:277-283.
9. Cheng GZ, Chan J, Wang Q, Zhang W, Sun CD, Wang LH. Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer research. 2007; 67:1979-1987.
10. Li QQ, Xu JD, Wang WJ, Cao XX, Chen Q, Tang F, Chen ZQ, Liu XP, Xu ZD. Twist1-mediated adriamycininduced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clinical cancer research: an official journal of the American Association for Cancer Research. 2009; 15:2657-2665.
11. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelialmesenchymal transitions in development and disease. Cell. 2009; 139:871-890.
12. Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, Popescu NC, Hahn WC, Weinberg RA. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes & development. 2001; 15:50-65.
13. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, Bell G, Guo W, Rubin J, Richardson AL, Weinberg RA. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell. 2011; 145:926-940.
14. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009; 138:645-659.
15. Tam WL, Lu H, Buikhuisen J, Soh BS, Lim E, Reinhardt F, Wu ZJ, Krall JA, Bierie B, Guo W, Chen X, Liu XS, Brown M, Lim B, Weinberg RA. Protein kinase C alpha is a central signaling node and therapeutic target for breast cancer stem cells. Cancer cell. 2013; 24:347-364.
16. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, Thompson CB. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell. 1993; 74:597-608.
17. Habens F, Lapham AS, Dallman CL, Pickering BM, Michels J, Marcusson EG, Johnson PW, Packham G. Distinct promoters mediate constitutive and inducible Bcl-XL expression in malignant lymphocytes. Oncogene. 2007; 26:1910-1919.
18. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Developmental cell. 2008; 14:818-829.
19. Santagata S, Thakkar A, Ergonul A, Wang B, Woo T, Hu R, Harrell JC, McNamara G, Schwede M, Culhane AC, Kindelberger D, Rodig S, Richardson A, Schnitt SJ, Tamimi RM, Ince TA. Taxonomy of breast cancer based on normal cell phenotype predicts outcome. The Journal of clinical investigation. 2014; 124:859-870.
20. Withers WA, Carruth FE. Gossypol-a Toxic Substance in Cottonseed. A Preliminary Note. Science. 1915; 41:324.
21. Kitada S, Leone M, Sareth S, Zhai D, Reed JC, Pellecchia M. Discovery, characterization, and structureactivity relationships studies of proapoptotic polyphenols targeting B-cell lymphocyte/leukemia-2 proteins. Journal of medicinal chemistry. 2003; 46:4259-4264.
22. Zhang M, Liu H, Guo R, Ling Y, Wu X, Li B, Roller PP, Wang S, Yang D. Molecular mechanism of gossypol-induced cell growth inhibition and cell death of HT-29 human colon carcinoma cells. Biochemical pharmacology. 2003; 66:93-103.
23. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, Willis SN, Scott CL, Day CL, Cory S, Adams JM, Roberts AW, Huang DC. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer cell. 2006; 10:389-399.
24. Degterev A, Lugovskoy A, Cardone M, Mulley B, Wagner G, Mitchison T, Yuan J. Identification of small-molecule inhibitors of interaction between the BH3 domain and Bcl-xL. Nature cell biology. 2001; 3:173-182.
25. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, Bruncko M, Deckwerth TL, Dinges J, Hajduk PJ, Joseph MK, Kitada S, Korsmeyer SJ, Kunzer AR, Letai A, Li C, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature. 2005; 435:677-681.
26. Tanida I, Ueno T, Kominami E. LC3 and Autophagy. Methods Mol Biol. 2008; 445:77-88.
27. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. The EMBO journal. 2000; 19:5720-5728.
28. Lian J, Wu X, He F, Karnak D, Tang W, Meng Y, Xiang D, Ji M, Lawrence TS, Xu L. A natural BH3 mimetic induces autophagy in apoptosis-resistant prostate cancer via modulating Bcl-2-Beclin1 interaction at endoplasmic reticulum. Cell death and differentiation. 2011; 18:60-71.
29. Olopade OI, Adeyanju MO, Safa AR, Hagos F, Mick R, Thompson CB, Recant WM. Overexpression of BCL-x protein in primary breast cancer is associated with high tumor grade and nodal metastases. The cancer journal from Scientific American. 1997; 3:230-237.
30. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nature reviews Cancer. 2005; 5:744-749.
31. de Herreros AG, Peiro S, Nassour M, Savagner P. Snail family regulation and epithelial mesenchymal transitions in breast cancer progression. Journal of mammary gland biology and neoplasia. 2010; 15:135-147.
32. Roxanis I. Occurrence and significance of epithelial-mesenchymal transition in breast cancer. Journal of clinical pathology. 2013; 66:517-521.
33. Luo J, Solimini NL, Elledge SJ. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell. 2009; 136:823-837.
34. Dobbelstein M, Moll U. Targeting tumour-supportive cellular machineries in anticancer drug development. Nature reviews Drug discovery. 2014; 13:179-196.
35. Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO, Brooks M, Reinhardt F, Su Y, Polyak K, Arendt LM, Kuperwasser C, Bierie B, Weinberg RA. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108:7950-7955.
36. Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature. 2013; 501:328-337.
37. Liedert B, Pluim D, Schellens J, Thomale J. Adductspecific monoclonal antibodies for the measurement of cisplatin-induced DNA lesions in individual cell nuclei. Nucleic acids research. 2006; 34:e47.
38. Ruifrok AC, Johnston DA. Quantification of histochemical staining by color deconvolution. Analytical and quantitative cytology and histology / the International Academy of Cytology [and] American Society of Cytology. 2001; 23:291-299.
39. Deverman BE, Cook BL, Manson SR, Niederhoff RA, Langer EM, Rosova I, Kulans LA, Fu X, Weinberg JS, Heinecke JW, Roth KA, Weintraub SJ. Bcl-xL deamidation is a critical switch in the regulation of the response to DNA damage. Cell. 2002; 111:51-62.