Doxycycline inhibits the cancer stem cell phenotype and epithelial-to-mesenchymal transition in breast cancer

Reference

• Wang D, Lu P, Zhang H, Luo M, Zhang X, Wei X, Gao J, Zhao Z, Liu C. Oct-4 and Nanog promote the epithelial-mesenchymal transition of breast cancer stem cells and are associated with poor prognosis in breast cancer patients. Oncotarget 2014; 5(21):10803; PMID:25301732; http://dx.doi.org/10.18632/oncotarget.2506
   PubMed Web of Science ®Google Scholar
• Siegel RL MK, Jemal A. Cancer statistics. CA Cancer J Clin 2016; 66(1):7–30; PMID:26742998; http://dx.doi.org/10.3322/caac.21332
   PubMed Web of Science ®Google Scholar
• Weigelt B, Peterse JL, Van't Veer LJ. Breast cancer metastasis: markers and models. Nat Rev Cancer 2005; 5(8):591–602; PMID:16056258; http://dx.doi.org/10.1038/nrc1670
   PubMed Web of Science ®Google Scholar
• Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA: Cancer J Clin 2011; 61(2):69–90; PMID:21296855
   PubMed Web of Science ®Google Scholar
• Jordan CT, Guzman ML, Noble M. Cancer stem cells. New Engl J Med 2006; 355(12):1253–61; PMID:16990388; http://dx.doi.org/10.1056/NEJMra061808
   PubMed Web of Science ®Google Scholar
• Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci 2003; 100(7):3983–8; http://dx.doi.org/10.1073/pnas.0530291100
   PubMed Web of Science ®Google Scholar
• Lamb R, Ozsvari B, Lisanti CL, Tanowitz HB, Howell A, Martinez-Outschoorn UE, Sotgia F, Lisanti MP. Antibiotics that target mitochondria effectively eradicate cancer stem cells, across multiple tumor types: Treating cancer like an infectious disease. Oncotarget 2015; 6(7): 4569–4584; PMID:25625193; http://dx.doi.org/10.18632/oncotarget.3174
   PubMed Web of Science ®Google Scholar
• Vlashi E, McBride WH, Pajonk F. Radiation responses of cancer stem cells. J Cell Biochem 2009; 108(2):339–342; PMID:19623582; http://dx.doi.org/10.1002/jcb.22275
   PubMedGoogle Scholar
• Phillips TM, McBride WH, Pajonk F. The response of CD24−/low/CD44+ breast cancer–initiating cells to radiation. J Natl Cancer Inst 2006; 98(24):1777–1785; PMID:17179479; http://dx.doi.org/10.1093/jnci/djj495
   PubMedGoogle Scholar
• Lagadec C, Vlashi E, Della Donna L, Meng Y, Dekmezian C, Kim K, Pajonk F. Survival and self-renewing capacity of breast cancer initiating cells during fractionated radiation treatment. Breast Cancer Res 2010; 12(1):1; http://dx.doi.org/10.1186/bcr2479
   Web of Science ®Google Scholar
• Lagadec C, Vlashi E, Della Donna L, Dekmezian C, Pajonk F. Radiation-induced reprogramming of breast cancer cells. Stem Cells 2012; 30(5):833–44; PMID:22489015; http://dx.doi.org/10.1002/stem.1058
   PubMed Web of Science ®Google Scholar
• Martin-Castillo B, Lopez-Bonet E, Cuyàs E, Viñas G, Pernas S, Dorca J, Menendez JA. Cancer stem cell-driven efficacy of trastuzumab (Herceptin): towards a reclassification of clinically HER2-positive breast carcinomas. Oncotarget 2015; 6(32):32317
   PubMed Web of Science ®Google Scholar
• Sarrio D, Franklin CK, Mackay A, Reis-Filho JS, Isacke CM. Epithelial and mesenchymal subpopulations within normal basal breast cell lines exhibit distinct stem cell/progenitor properties. Stem Cells 2012; 30(2):292–303; PMID:22102611; http://dx.doi.org/10.1002/stem.791
   PubMedGoogle Scholar
• Liu S, Cong Y, Wang D, Sun Y, Deng L, Liu Y, Martin-Trevino R, Shang L, McDermott SP, Landis MD, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Rep 2014; 2(1):78–91; PMID:24511467; http://dx.doi.org/10.1016/j.stemcr.2013.11.009
   PubMed Web of Science ®Google Scholar
• Federici TJ. The non-antibiotic properties of tetracyclines: clinical potential in ophthalmic disease. Pharmacol Res 2011; 64(6): 614–623; PMID:21843641; http://dx.doi.org/10.1016/j.phrs.2011.06.013
   PubMedGoogle Scholar
• Griffin MO, Ceballos G, Villarreal FJ. Tetracycline compounds with non-antimicrobial organ protective properties: possible mechanisms of action. Pharmacol Res 2011; 63(2): 102–107; PMID:20951211; http://dx.doi.org/10.1016/j.phrs.2010.10.004
   PubMed Web of Science ®Google Scholar
• Garrido-Mesa N, Zarzuelo A, Galvez J. ( 2013) Minocycline: far beyond an antibiotic. Br J Pharmacol 2013; 169(2): 337–352; PMID:23441623; http://dx.doi.org/10.1111/bph.12139
   PubMed Web of Science ®Google Scholar
• Saikali Z, Singh G. Doxycycline and other tetracyclines in the treatment of bone metastasis. Anti-Cancer Drugs 2003; 14(10):773–8; PMID:14597870
   PubMedGoogle Scholar
• Newby AC. Matrix metalloproteinase inhibition therapy for vascular diseases. Vasc Pharmacol 2012; 56(5): 232–244; PMID:22326338
   PubMed Web of Science ®Google Scholar
• Vlashi E, Lagadec C, Vergnes L, Reue K, Frohnen P, Chan M, Alhiyari Y, Dratver MB, Pajonk F. Metabolic differences in breast cancer stem cells and differentiated progeny. Breast Cancer Res Treatment 2014; 146(3):525–534; PMID:25007966; http://dx.doi.org/10.1007/s10549-014-3051-2
   PubMedGoogle Scholar
• Lamb R, Harrison H, Hulit J, Smith DL, Lisanti MP, Sotgia F. Mitochondria as new therapeutic targets for eradicating cancer stem cells: Quantitative proteomics and functional validation via MCT1/2 inhibition. Oncotarget 2014; 5(22): 11029–11037; PMID:25415228; http://dx.doi.org/10.18632/oncotarget.2789
   PubMed Web of Science ®Google Scholar
• Vinogradov S, Wei X. Cancer stem cells and drug resistance: the potential of nanomedicine. Nanomedicine 2012; 7(4):597–615; http://dx.doi.org/10.2217/nnm.12.22
   PubMed Web of Science ®Google Scholar
• Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005; 65(13):5506–5511; PMID:15994920; http://dx.doi.org/10.1158/0008-5472.CAN-05-0626
   PubMed Web of Science ®Google Scholar
• Bozorgi A, Khazaei M, Khazaei MR. New findings on breast cancer stem cells: a review. J Breast Cancer 2015; 18(4):303–312; PMID:26770236; http://dx.doi.org/10.4048/jbc.2015.18.4.303
   PubMedGoogle Scholar
• Shaw LM. Tumor cell invasion assays. Cell Migration: Dev Methods Protocols 2005:97–105.
   Google Scholar
• Kim MJ, Kim HS, Lee SH, Yang Y, Lee MS, Lim JS. NDRG2 controls COX-2/PGE2-mediated breast cancer cell migration and invasion. Mol Cells 2014; 37(10): 759–765; PMID:25256221; http://dx.doi.org/10.14348/molcells.2014.0232
   PubMed Web of Science ®Google Scholar
• Hayashida T, Jinno H, Kitagawa Y, Kitajima M. Cooperation of cancer stem cell properties and epithelial-mesenchymal transition in the establishment of breast cancer metastasis. J Oncol 2011; 2011:591427; http://dx.doi.org/10.1155/2011/591427
   PubMedGoogle Scholar
• Meng J, Sun B, Zhao X, Zhang D, Zhao X, Gu Q, Dong X, Zhao N, Liu P, Liu Y. Doxycycline as an Inhibitor of the Epithelial-to-Mesenchymal Transition and Vasculogenic Mimicry in Hepatocellular Carcinoma. Mol Cancer Ther 2014; 3(12): 3107–3122; http://dx.doi.org/10.1158/1535-7163.MCT-13-1060
   Google Scholar
• Ding Y, Yu AQ, Li CL, Fang J, Zeng Y, Li DS. TALEN-mediated Nanog disruption results in less invasiveness, more chemosensitivity and reversal of EMT in Hela cells. Oncotarget 2014; 5(18): 8393–8401; PMID:25245189; http://dx.doi.org/10.18632/oncotarget.2298
   PubMed Web of Science ®Google Scholar
• Ogier-Denis E, Codogno P. Autophagy: a barrier or an adaptive response to cancer. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer 2003; 1603(2):113–28; http://dx.doi.org/10.1016/S0304-419X(03)00004-0
   PubMed Web of Science ®Google Scholar
• Chen S, Jiang YZ, Huang L, Zhou RJ, Yu KD, Liu Y, Shao ZM. The residual tumor autophagy marker LC3B serves as a prognostic marker in local advanced breast cancer after neoadjuvant chemotherapy. Clin Cancer Res 2013; 19(24): 6853–6862; http://dx.doi.org/10.1158/1078-0432.CCR-13-1617
   PubMed Web of Science ®Google Scholar
• Lazova R, Camp RL, Klump V, Siddiqui SF, Amaravadi RK, Pawelek JM. Punctate LC3B expression is a common feature of solid tumors and associated with proliferation, metastasis, and poor outcome. Clin Cancer Res 2012; 18(2): 370–379; PMID:22080440; http://dx.doi.org/10.1158/1078-0432.CCR-11-1282
   PubMed Web of Science ®Google Scholar
• Yang MC, Wang HC, Hou YC, Tung HL, Chiu TJ, Shan YS. Blockade of autophagy reduces pancreatic cancer stem cell activity and potentiates the tumoricidal effect of gemcitabine. Mol Cancer 2015; 14(1):1; PMID:25560632; http://dx.doi.org/10.1186/1476-4598-14-1
   PubMedGoogle Scholar
• Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451(7182):1069–75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
   PubMed Web of Science ®Google Scholar
• Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2− cancer cells are similarly tumorigenic. Cancer Res 2005; 65(14):6207–6219; PMID:16024622; http://dx.doi.org/10.1158/0008-5472.CAN-05-0592
   PubMed Web of Science ®Google Scholar
• Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005; 65(13):5506–5511; PMID:15994920; http://dx.doi.org/10.1158/0008-5472.CAN-05-0626
   PubMed Web of Science ®Google Scholar
• Vlashi E, Lagadec C, Chan M, Frohnen P, McDonald AJ, Pajonk F. Targeted elimination of breast cancer cells with low proteasome activity is sufficient for tumor regression. Breast Cancer Res Treatment 2013; 141(2): 197–203; PMID:24013708; http://dx.doi.org/10.1007/s10549-013-2688-6
   PubMedGoogle Scholar
• Ciavardelli D, Rossi C, Barcaroli D, Volpe S, Consalvo A, Zucchelli M, De Cola A, Scavo E, Carollo R, D'Agostino D, et al. Breast cancer stem cells rely on fermentative glycolysis and are sensitive to 2-deoxyglucose treatment. Cell Death Dis 2014; 5(7): e1336
   PubMedGoogle Scholar
• Feng W, Gentles A, Nair RV, Huang M, Lin Y, Lee CY, Cai S, Scheeren FA, Kuo AH, Diehn M. Targeting unique metabolic properties of breast tumor initiating cells. Stem Cells 2014; 32(7): 1734–1745; PMID:24497069; http://dx.doi.org/10.1002/stem.1662
   PubMedGoogle Scholar
• Vlashi E, Lagadec C, Vergnes L, Matsutani T, Masui K, Poulou M, Popescu R, Della Donna L, Evers P, Dekmezian C, et al. Metabolic state of glioma stem cells and nontumorigenic cells. Proc Nat Acad Sci 2011; 108(38): 16062–16067; http://dx.doi.org/10.1073/pnas.1106704108
   PubMed Web of Science ®Google Scholar
• Qin Y, Zhang Q, Lee S, Zhong WL, Liu YR, Liu HJ, Zhao D, Chen S, Xiao T, Meng J, et al. Doxycycline reverses epithelial-to-mesenchymal transition and suppresses the proliferation and metastasis of lung cancer cells. Oncotarget 2015; 6(38):40667; PMID:26512779
   PubMed Web of Science ®Google Scholar
• Wan L, Dong H, Huo Xu JM, Zhu Y, Lu Y, Wang J, Zhang T, Li T, Xie J, Xu B, et al. Aspirin, lysine, mifepristone and doxycycline combined can effectively and safely prevent and treat cancer metastasis: prevent seeds from gemmating on soil. Oncotarget 2015; 6(34):35157; PMID:26459390
   PubMed Web of Science ®Google Scholar
• Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gélinas C, Fan Y, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006; 10(1): 51–64; PMID:16843265; http://dx.doi.org/10.1016/j.ccr.2006.06.001
   PubMed Web of Science ®Google Scholar
• Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, Thompson CB. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 2005; 120(2): 237–248; PMID:15680329; http://dx.doi.org/10.1016/j.cell.2004.11.046
   PubMed Web of Science ®Google Scholar
• Cufí S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Vellon L, Menendez JA. Autophagy positively regulates the CD44+ CD24-/low breast cancer stem-like phenotype. Cell Cycle 2011; 10(22): 3871–3885; http://dx.doi.org/10.4161/cc.10.22.17976
   PubMed Web of Science ®Google Scholar
• Maycotte P, Jones KL, Goodall ML, Thorburn J, Thorburn A. Autophagy Supports Breast Cancer Stem Cell Maintenance by Regulating IL6 Secretion. Mol Cancer Res 2015; 13(4):651–658; http://dx.doi.org/10.1158/1541-7786.MCR-14-0487
   PubMed Web of Science ®Google Scholar
• Gong C, Bauvy C, Tonelli G, Yue W, Delomenie C, Nicolas V, Zhu Y, Domergue V, Marin-Esteban V, Tharinger H, et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene 2013; 32(18): 2261–2272; PMID:22733132; http://dx.doi.org/10.1038/onc.2012.252
   PubMed Web of Science ®Google Scholar
• Guan JL, Simon AK, Prescott M, Menendez JA, Liu F, Wang F, Wang C, Wolvetang E, Vazquez-Martin A, Zhang J. Autophagy in stem cells. Autophagy 2013; 9(6):830–49; PMID:23486312; http://dx.doi.org/10.4161/auto.24132
   PubMed Web of Science ®Google Scholar
• Gong C, Song E, Codogno P, Mehrpour M. The roles of BECN1 and autophagy in cancer are context dependent. Autophagy 2012; 8:1853–5; PMID:22960473; http://dx.doi.org/10.4161/auto.21996
   PubMed Web of Science ®Google Scholar
• Lamb R, Fiorillo M, Chadwick A, Ozsvari B, Reeves KJ, Smith DL, Clarke RB, Howell SJ, Cappello AR, Martinez-Outschoorn UE, et al. Doxycycline down-regulates DNA-PK and radiosensitizes tumor initiating cells: Implications for more effective radiation therapy. Oncotarget 2015; 6(16): 14005; PMID:26087309; http://dx.doi.org/10.18632/oncotarget.4159
   PubMed Web of Science ®Google Scholar
• Pulvino M, Chen L, Oleksyn D, Li J, Compitello G, Rossi R, Spence S, Balakrishnan V, Jordan C, Poligone B, et al. Inhibition of COP9-signalosome (CSN) deneddylating activity and tumor growth of diffuse large B-cell lymphomas by doxycycline. Oncotarget 2015; 6(17):14796; PMID:26142707; http://dx.doi.org/10.18632/oncotarget.4193
   PubMedGoogle Scholar