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Breast Cancer Proteome Takes More Than Two to Tango on TRAIL: Beat Them at Their Own Game

  • Topical Review
  • Published:
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Abstract

Breast carcinogenesis is a multidimensional disease that has resisted drug-related solutions to date because of heterogeneity, disorganized spatiotemporal behavior of signal transduction cascades, cell cycle checkpoints, cell transition, plasticity, and impaired pro-apoptotic response. These synchronized oncogenic events, including protein–protein interaction, transcriptional–regulatory, and signaling networks, trigger genomic and transcriptional disturbances in TRAIL-mediated signaling network neighborhoods. Therefore, tumor cells often acquire the ability to escape death by suppressing cell death pathways that normally function to eliminate damaged and harmful cells. This review describes the TRAIL-mediated cell death signaling pathways, the interactions between these pathways, and the ways in which these pathways are deregulated in breast cancer.

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References

  • Allensworth JL, Aird KM, Aldrich AJ, Batinic-Haberle I, Devi GR (2012) XIAP inhibition and generation of reactive oxygen species enhances TRAIL sensitivity in inflammatory breast cancer cells. Mol Cancer Ther 11:1518–1527

    Article  PubMed  CAS  Google Scholar 

  • Amm HM, Buchsbaum DJ (2011) Relationship between galectin-3 expression and TRAIL sensitivity in breast cancer. Expert Rev Anticancer Ther 11:1193–1196

    Article  PubMed  CAS  Google Scholar 

  • Amm HM, Zhou T, Steg AD, Kuo H, Li Y, Buchsbaum DJ (2011) Mechanisms of drug sensitization to TRA-8, an agonistic death receptor 5 antibody, involve modulation of the intrinsic apoptotic pathway in human breast cancer cells. Mol Cancer Res 9:403–417

    Article  PubMed  CAS  Google Scholar 

  • Austin CD, Lawrence DA, Peden AA, Varfolomeev EE, Totpal K, De Mazière AM, Klumperman J, Arnott D, Pham V, Scheller RH, Ashkenazi A (2006) Death-receptor activation halts clathrin-dependent endocytosis. Proc Natl Acad Sci USA 103:10283–10288

    Article  PubMed  CAS  Google Scholar 

  • Bae S, Ma K, Kim TH, Lee ES, Oh KT, Park ES, Lee KC, Youn YS (2012) Doxorubicin-loaded human serum albumin nanoparticles surface-modified with TNF-related apoptosis-inducing ligand and transferrin for targeting multiple tumor types. Biomaterials 33:1536–1546

    Article  PubMed  CAS  Google Scholar 

  • Bolanz KA, Hediger MA, Landowski CP (2008) The role of TRPV6 in breast carcinogenesis. Mol Cancer Ther 7:271–279

    Article  PubMed  CAS  Google Scholar 

  • Bolanz KA, Kovacs GG, Landowski CP, Hediger MA (2009) Tamoxifen inhibits TRPV6 activity via estrogen receptor-independent pathways in TRPV6-expressing MCF-7 breast cancer cells. Mol Cancer Res 7:2000–2010

    Article  PubMed  CAS  Google Scholar 

  • Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447

    Article  PubMed  CAS  Google Scholar 

  • Chen Q, Zhang XH, Massagué J (2011) Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 20:538–549

    Article  PubMed  CAS  Google Scholar 

  • Chodon D, Guilbert A, Dhennin-Duthille I, Gautier M, Telliez MS, Sevestre H, Ouadid-Ahidouch H (2010) Estrogen regulation of TRPM8 expression in breast cancer cells. BMC Cancer 10:212

    Article  PubMed  CAS  Google Scholar 

  • Dhennin-Duthille I, Gautier M, Faouzi M, Guilbert A, Brevet M, Vaudry D, Ahidouch A, Sevestre H, Ouadid-Ahidouch H (2011) High expression of transient receptor potential channels in human breast cancer epithelial cells and tissues: correlation with pathological parameters. Cell Physiol Biochem 28:813–822

    Article  PubMed  CAS  Google Scholar 

  • Ding B, Wu X, Fan W, Wu Z, Gao J, Zhang W, Ma L, Xiang W, Zhu Q, Liu J, Ding X, Gao S (2011) Anti-DR5 monoclonal antibody–mediated DTIC-loaded nanoparticles combining chemotherapy and immunotherapy for malignant melanoma: target formulation development and in vitro anticancer activity. Int J Nanomed 6:1991–2005

    CAS  Google Scholar 

  • Ding J, Polier G, Köhler R, Giaisi M, Krammer PH, Li-Weber M (2012) Wogonin and related natural flavones overcome tumor necrosis factor–related apoptosis-inducing ligand (TRAIL) protein resistance of tumors by down-regulation of c-FLIP protein and up-regulation of TRAIL receptor 2 expression. J Biol Chem 287:641–649

    Article  PubMed  CAS  Google Scholar 

  • Dong Y, Yin S, Li J, Jiang C, Ye M, Hu H (2011) Bufadienolide compounds sensitize human breast cancer cells to TRAIL-induced apoptosis via inhibition of STAT3/Mcl-1 pathway. Apoptosis 16:394–403

    Article  PubMed  CAS  Google Scholar 

  • Dong LF, Grant G, Massa H, Zobalova R, Akporiaye E, Neuzil J (2012) α-Tocopheryloxyacetic acid is superior to α-tocopheryl succinate in suppressing HER2-high breast carcinomas due to its higher stability. Int J Cancer 131:1052–1058

    Article  PubMed  CAS  Google Scholar 

  • Ehrenschwender M, Siegmund D, Wicovsky A, Kracht M, Dittrich-Breiholz O, Spindler V, Waschke J, Kalthoff H, Trauzold A, Wajant H (2010) Mutant PIK3CA licenses TRAIL and CD95L to induce non-apoptotic caspase-8-mediated ROCK activation. Cell Death Differ 17:1435–1447

    Article  PubMed  CAS  Google Scholar 

  • El Hiani Y, Ahidouch A, Lehen’kyi V, Hague F, Gouilleux F, Mentaverri R, Kamel S, Lassoued K, Brûlé G, Ouadid-Ahidouch H (2009) Extracellular signal–regulated kinases 1 and 2 and TRPC1 channels are required for calcium-sensing receptor-stimulated MCF-7 breast cancer cell proliferation. Cell Physiol Biochem 23:335–346

    Article  PubMed  CAS  Google Scholar 

  • Ellison-Zelski SJ, Alarid ET (2010) Maximum growth and survival of estrogen receptor-alpha positive breast cancer cells requires the Sin3A transcriptional repressor. Mol Cancer 9:263

    Article  PubMed  CAS  Google Scholar 

  • Engel JB, Martens T, Hahne JC, Häusler SF, Krockenberger M, Segerer S, Djakovic A, Meyer S, Dietl J, Wischhusen J, Honig A (2012) Effects of lobaplatin as a single agent and in combination with TRAIL on the growth of triple-negative p53-mutated breast cancers in vitro. Anticancer Drugs 23:426–436

    Article  PubMed  CAS  Google Scholar 

  • Fan H, Hu QD, Xu FJ, Liang WQ, Tang GP, Yang WT (2012) In vivo treatment of tumors using host–guest conjugated nanoparticles functionalized with doxorubicin and therapeutic gene pTRAIL. Biomaterials 33:1428–1436

    Article  PubMed  CAS  Google Scholar 

  • Farooqi AA, Javeed MK, Javed Z, Riaz AM, Mukhtar S, Minhaj S, Abbas S, Bhatti S (2011) TRPM channels: same ballpark, different players, and different rules in immunogenetics. Immunogenetics 63:773–787

    Article  PubMed  Google Scholar 

  • Fiorio Pla A, Ong HL, Cheng KT, Brossa A, Bussolati B, Lockwich T, Paria B, Munaron L, Ambudkar IS (2012) TRPV4 mediates tumor-derived endothelial cell migration via arachidonic acid–activated actin remodeling. Oncogene 31:200–212

    Article  PubMed  CAS  Google Scholar 

  • Ganai S, Arenas RB, Forbes NS (2009) Tumour-targeted delivery of TRAIL using Salmonella typhimurium enhances breast cancer survival in mice. Br J Cancer 101:1683–1691

    Article  PubMed  CAS  Google Scholar 

  • Gao ZG, Tian L, Hu J, Park IS, Bae YH (2011) Prevention of metastasis in a 4T1 murine breast cancer model by doxorubicin carried by folate conjugated pH sensitive polymeric micelles. J Control Release 152:84–89

    Article  PubMed  CAS  Google Scholar 

  • Garimella SV, Rocca A, Lipkowitz S (2012) WEE1 inhibition sensitizes basal breast cancer cells to TRAIL-induced apoptosis. Mol Cancer Res 10:75–85

    Article  PubMed  CAS  Google Scholar 

  • Gasparian ME, Domnina LV, Ivanova OY, Izyumov DS, Lomakin AY, Popova EN, Yagolovich AV, Pletjushkina OY, Dolgikh DA, Chernyak BV (2008) Cytoskeleton inhibitors combined with TRAIL induce apoptosis in HeLa carcinoma cells overexpressing antiapoptotic protein Bcl-2. Biochemistry (Mosc) 73:358–362

    Article  CAS  Google Scholar 

  • Grisendi G, Bussolari R, Cafarelli L, Petak I, Rasini V, Veronesi E, De Santis G, Spano C, Tagliazzucchi M, Barti-Juhasz H, Scarabelli L, Bambi F, Frassoldati A, Rossi G, Casali C, Morandi U, Horwitz EM, Paolucci P, Conte P, Dominici M (2010) Adipose-derived mesenchymal stem cells as stable source of tumor necrosis factor–related apoptosis-inducing ligand delivery for cancer therapy. Cancer Res 70:3718–3729

    Article  PubMed  CAS  Google Scholar 

  • Guilbert A, Dhennin-Duthille I, Hiani YE, Haren N, Khorsi H, Sevestre H, Ahidouch A, Ouadid-Ahidouch H (2008) Expression of TRPC6 channels in human epithelial breast cancer cells. BMC Cancer 8:125

    Article  PubMed  CAS  Google Scholar 

  • Guilbert A, Gautier M, Dhennin-Duthille I, Haren N, Sevestre H, Ouadid-Ahidouch H (2009) Evidence that TRPM7 is required for breast cancer cell proliferation. Am J Physiol Cell Physiol 297:C493–C502

    Article  PubMed  CAS  Google Scholar 

  • Guo SY, Liu SG, Liu L, Zhou XJ, Gu Y (2012) RNAi silencing of the MEKK3 gene promotes TRAIL-induced apoptosis in MCF-7 cells and suppresses the transcriptional activity of NF-κB. Oncol Rep 27:441–446

    PubMed  CAS  Google Scholar 

  • Hafid SR, Radhakrishnan AK, Nesaretnam K (2010) Tocotrienols are good adjuvants for developing cancer vaccines. BMC Cancer 10:5

    Article  PubMed  CAS  Google Scholar 

  • Hahn T, Fried K, Hurley LH, Akporiaye ET (2009) Orally active alpha-tocopheryloxyacetic acid suppresses tumor growth and multiplicity of spontaneous murine breast cancer. Mol Cancer Ther 8:1570–1578

    Article  PubMed  CAS  Google Scholar 

  • Hahn T, Bradley-Dunlop DJ, Hurley LH, Von-Hoff D, Gately S, Mary DL, Lu H, Penichet ML, Besselsen DG, Cole BB, Meeuwsen T, Walker E, Akporiaye ET (2011) The vitamin E analog, alpha-tocopheryloxyacetic acid enhances the anti-tumor activity of trastuzumab against HER2/neu-expressing breast cancer. BMC Cancer 11:471

    Article  PubMed  CAS  Google Scholar 

  • Han L, Huang R, Li J, Liu S, Huang S, Jiang C (2011) Plasmid pORF-hTRAIL and doxorubicin co-delivery targeting to tumor using peptide-conjugated polyamidoamine dendrimer. Biomaterials 32:1242–1252

    Article  PubMed  CAS  Google Scholar 

  • Holland PM, Miller R, Jones J, Douangpanya H, Piasecki J, Roudier M, Dougall WC (2010) Combined therapy with the RANKL inhibitor RANK-Fc and rhApo2L/TRAIL/dulanermin reduces bone lesions and skeletal tumor burden in a model of breast cancer skeletal metastasis. Cancer Biol Ther 9:539–550

    Article  PubMed  CAS  Google Scholar 

  • Hoogwater FJ, Nijkamp MW, Smakman N, Steller EJ, Emmink BL, Westendorp BF, Raats DA, Sprick MR, Schaefer U, Van Houdt WJ, De Bruijn MT, Schackmann RC, Derksen PW, Medema JP, Walczak H, Borel Rinkes IH, Kranenburg O (2010) Oncogenic K-Ras turns death receptors into metastasis-promoting receptors in human and mouse colorectal cancer cells. Gastroenterology 138:2357–2367

    Article  PubMed  CAS  Google Scholar 

  • Hsieh TC, Wu JM (2008) Suppression of cell proliferation and gene expression by combinatorial synergy of EGCG, resveratrol and gamma-tocotrienol in estrogen receptor-positive MCF-7 breast cancer cells. Int J Oncol 33:851–859

    PubMed  CAS  Google Scholar 

  • Huang L, Chen H, Zheng Y, Song X, Liu R, Liu K, Zeng X, Mei L (2011) Nanoformulation of d-α-tocopheryl polyethylene glycol 1000 succinate-b-poly(ε-caprolactone-ran-glycolide) diblock copolymer for breast cancer therapy. Integr Biol (Camb) 3:993–1002

    Article  CAS  Google Scholar 

  • Jang JY, Jeon YK, Choi Y, Kim CW (2010) Short-hairpin RNA-induced suppression of adenine nucleotide translocase-2 in breast cancer cells restores their susceptibility to TRAIL-induced apoptosis by activating JNK and modulating TRAIL receptor expression. Mol Cancer 9:262

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Chen K, Tang Z, Zeng Z, Yao W, Sun D, Ka W, He D, Wen Z, Chien S (2006) TRAIL gene reorganizes the cytoskeleton and decreases the motility of human leukemic Jurkat cells. Cell Motil Cytoskeleton 63:471–482

    Article  PubMed  CAS  Google Scholar 

  • Jin Z, McDonald ER 3rd, Dicker DT, El-Deiry WS (2004) Deficient tumor necrosis factor–related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis. J Biol Chem 279:35829–35839

    Article  PubMed  CAS  Google Scholar 

  • Kajitani K, Tanaka Y, Arihiro K, Kataoka T, Ohdan H (2012) Mechanistic analysis of the antitumor efficacy of human natural killer cells against breast cancer cells. Breast Cancer Res Treat 134:139–155

    Article  PubMed  Google Scholar 

  • Kawabata A, Baoum A, Ohta N, Jacquez S, Seo GM, Berkland C, Tamura M (2012) Intratracheal administration of a nanoparticle-based therapy with the angiotensin II type 2 receptor gene attenuates lung cancer growth. Cancer Res 72:2057–2067

    Article  PubMed  CAS  Google Scholar 

  • Kim M, Liao J, Dowling ML, Voong KR, Parker SE, Wang S, El-Deiry WS, Kao GD (2008) TRAIL inactivates the mitotic checkpoint and potentiates death induced by microtubule-targeting agents in human cancer cells. Cancer Res 68:3440–3449

    Article  PubMed  CAS  Google Scholar 

  • Kim DY, Kim MJ, Kim HB, Lee JW, Bae JH, Kim DW, Kang CD, Kim SH (2011a) Suppression of multidrug resistance by treatment with TRAIL in human ovarian and breast cancer cells with high level of c-Myc. Biochim Biophys Acta 1812:796–805

    Article  PubMed  CAS  Google Scholar 

  • Kim TH, Jiang HH, Youn YS, Park CW, Lim SM, Jin CH, Tak KK, Lee HS, Lee KC (2011b) Preparation and characterization of Apo2L/TNF-related apoptosis-inducing ligand-loaded human serum albumin nanoparticles with improved stability and tumor distribution. J Pharm Sci 100:482–491

    Article  PubMed  CAS  Google Scholar 

  • Kisim A, Atmaca H, Cakar B, Karabulut B, Sezgin C, Uzunoglu S, Uslu R, Karaca B (2012) Pretreatment with AT-101 enhances tumor necrosis factor–related apoptosis-inducing ligand (TRAIL)-induced apoptosis of breast cancer cells by inducing death receptors 4 and 5 protein levels. J Cancer Res Clin Oncol 138:1155–1163

    Article  PubMed  CAS  Google Scholar 

  • Kohlhaas SL, Craxton A, Sun XM, Pinkoski MJ, Cohen GM (2007) Receptor-mediated endocytosis is not required for TRAIL-induced apoptosis. J Biol Chem 282:12831–12841

    Article  PubMed  CAS  Google Scholar 

  • Lagadec C, Adriaenssens E, Toillon RA, Chopin V, Romon R, Van Coppenolle F, Hondermarck H, Le Bourhis X (2008) Tamoxifen and TRAIL synergistically induce apoptosis in breast cancer cells. Oncogene 27:1472–1477

    Article  PubMed  CAS  Google Scholar 

  • Lakshmanan I, Ponnusamy MP, Das S, Chakraborty S, Haridas D, Mukhopadhyay P, Lele SM, Batra SK (2012) MUC16 induced rapid G2/M transition via interactions with JAK2 for increased proliferation and anti-apoptosis in breast cancer cells. Oncogene 31:805–817

    Article  PubMed  CAS  Google Scholar 

  • Landowski CP, Bolanz KA, Suzuki Y, Hediger MA (2011) Chemical inhibitors of the calcium entry channel TRPV6. Pharm Res 28:322–330

    Article  PubMed  CAS  Google Scholar 

  • Latimer P, Menchaca M, Snyder RM, Yu W, Gilbert BE, Sanders BG, Kline K (2009) Aerosol delivery of liposomal formulated paclitaxel and vitamin E analog reduces murine mammary tumor burden and metastases. Exp Biol Med (Maywood) 234:1244–1252

    Article  CAS  Google Scholar 

  • Lee YJ, Song YK, Song JJ, Siervo-Sassi RR, Kim HR, Li L, Spitz DR, Lokshin A, Kim JH (2003) Reconstitution of galectin-3 alters glutathione content and potentiates TRAIL-induced cytotoxicity by dephosphorylation of Akt. Exp Cell Res 288:21–34

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Yagita H, Sayers TJ, Celis E (2010) Optimized combination therapy using bortezomib, TRAIL and TLR agonists in established breast tumors. Cancer Immunol Immunother 59:1073–1081

    Article  PubMed  CAS  Google Scholar 

  • Lee AL, Dhillon SH, Wang Y, Pervaiz S, Fan W, Yang YY (2011a) Synergistic anti-cancer effects via co-delivery of TNF-related apoptosis-inducing ligand (TRAIL/Apo2L) and doxorubicin using micellar nanoparticles. Mol Biosyst 7:1512–1522

    Article  PubMed  CAS  Google Scholar 

  • Lee AL, Wang Y, Pervaiz S, Fan W, Yang YY (2011b) Synergistic anticancer effects achieved by co-delivery of TRAIL and paclitaxel using cationic polymeric micelles. Macromol Biosci 11:296–307

    Article  PubMed  CAS  Google Scholar 

  • Leong S, McKay MJ, Christopherson RI, Baxter RC (2012) Biomarkers of breast cancer apoptosis induced by chemotherapy and TRAIL. J Proteome Res 11:1240–1250

    Article  PubMed  CAS  Google Scholar 

  • Li M, Knight DA, Smyth MJ, Stewart TJ (2012) Sensitivity of a novel model of mammary cancer stem cell-like cells to TNF-related death pathways. Cancer Immunol Immunother 61:1255–1268

    Article  PubMed  CAS  Google Scholar 

  • Lim SM, Kim TH, Jiang HH, Park CW, Lee S, Chen X, Lee KC (2011) Improved biological half-life and anti-tumor activity of TNF-related apoptosis-inducing ligand (TRAIL) using PEG-exposed nanoparticles. Biomaterials 32:3538–3546

    Article  PubMed  CAS  Google Scholar 

  • Lin CI, Whang EE, Abramson MA, Donner DB, Bertagnolli MM, Moore FD Jr, Ruan DT (2009) Galectin-3 regulates apoptosis and doxorubicin chemoresistance in papillary thyroid cancer cells. Biochem Biophys Res Commun 379:626–631

    Article  PubMed  CAS  Google Scholar 

  • Lin T, Ding Z, Li N, Xu J, Luo G, Liu J, Shen J (2011a) 2-Tellurium-bridged β-cyclodextrin, a thioredoxin reductase inhibitor, sensitizes human breast cancer cells to TRAIL-induced apoptosis through DR5 induction and NF-κB suppression. Carcinogenesis 32:154–167

    Article  PubMed  CAS  Google Scholar 

  • Lin T, Ding Z, Li N, Xu J, Luo G, Liu J, Shen J (2011b) Seleno-cyclodextrin sensitises human breast cancer cells to TRAIL-induced apoptosis through DR5 induction and NF-κB suppression. Eur J Cancer 47:1890–1907

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Li J, Huang Y, Huang C (2012a) Inhibition of transient receptor potential melastain 7 channel increases HSCs apoptosis induced by TRAIL. Life Sci 90:612–618

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Zhang W, Jiang M, Zhang Y, Liu S, Liu Y, Zheng D (2012b) Adeno-associated virus-mediated doxycycline-regulatable TRAIL expression suppresses growth of human breast carcinoma in nude mice. BMC Cancer 12:153

    Article  CAS  Google Scholar 

  • Londoño-Joshi AI, Oliver PG, Li Y, Lee CH, Forero-Torres A, Lobuglio AF, Buchsbaum DJ (2012) Basal-like breast cancer stem cells are sensitive to anti-DR5 mediated cytotoxicity. Breast Cancer Res Treat 133:437–445

    Article  PubMed  CAS  Google Scholar 

  • Lu J, McEachern D, Sun H, Bai L, Peng Y, Qiu S, Miller R, Liao J, Yi H, Liu M, Bellail A, Hao C, Sun SY, Ting AT, Wang S (2011) Therapeutic potential and molecular mechanism of a novel, potent, nonpeptide, Smac mimetic SM-164 in combination with TRAIL for cancer treatment. Mol Cancer Ther 10:902–914

    Article  PubMed  CAS  Google Scholar 

  • Maginn EN, Browne PV, Hayden P, Vandenberghe E, MacDonagh B, Evans P, Goodyer M, Tewari P, Campiani G, Butini S, Williams DC, Zisterer DM, Lawler MP, McElligott AM (2011) PBOX-15, a novel microtubule targeting agent, induces apoptosis, upregulates death receptors, and potentiates TRAIL-mediated apoptosis in multiple myeloma cells. Br J Cancer 104:281–289

    Article  PubMed  CAS  Google Scholar 

  • Malin D, Chen F, Schiller C, Koblinski J, Cryns VL (2011) Enhanced metastasis suppression by targeting TRAIL receptor 2 in a murine model of triple-negative breast cancer. Clin Cancer Res 17:5005–5015

    Article  PubMed  CAS  Google Scholar 

  • Mazurek N, Sun YJ, Liu KF, Gilcrease MZ, Schober W, Nangia-Makker P, Raz A, Bresalier RS (2007) Phosphorylated galectin-3 mediates tumor necrosis factor–related apoptosis-inducing ligand signaling by regulating phosphatase and tensin homologue deleted on chromosome 10 in human breast carcinoma cells. J Biol Chem 282:21337–21348

    Article  PubMed  CAS  Google Scholar 

  • Mazurek N, Byrd JC, Sun Y, Ueno S, Bresalier RS (2011) A galectin-3 sequence polymorphism confers TRAIL sensitivity to human breast cancer cells. Cancer 117:4375–4380

    Article  PubMed  CAS  Google Scholar 

  • Mazurek N, Byrd JC, Sun Y, Hafley M, Ramirez K, Burks J, Bresalier RS (2012) Cell-surface galectin-3 confers resistance to TRAIL by impeding trafficking of death receptors in metastatic colon adenocarcinoma cells. Cell Death Differ 19:523–533

    Article  PubMed  CAS  Google Scholar 

  • Meng X, Brachova P, Yang S, Xiong Z, Zhang Y, Thiel KW, Leslie KK (2011) Knockdown of MTDH sensitizes endometrial cancer cells to cell death induction by death receptor ligand TRAIL and HDAC inhibitor LBH589 co-treatment. PLoS One 6:e20920

    Article  PubMed  CAS  Google Scholar 

  • Miao L, Zhang K, Qiao C, Jin X, Zheng C, Yang B, Sun H (2012) Antitumor effect of human TRAIL on adenoid cystic carcinoma using magnetic nanoparticle mediated gene expression. Nanomedicine. doi:10.1016/j.nano.2012.04.006

  • Min KJ, Jang JH, Lee JT, Choi KS, Kwon TK (2012) Glucocorticoid receptor antagonist sensitizes TRAIL-induced apoptosis in renal carcinoma cells through up-regulation of DR5 and down-regulation of c-FLIP(L) and Bcl-2. J Mol Med (Berl) 90:309–319

    Article  CAS  Google Scholar 

  • Myc A, Kukowska-Latallo J, Cao P, Swanson B, Battista J, Dunham T, Baker JR Jr (2010) Targeting the efficacy of a dendrimer-based nanotherapeutic in heterogeneous xenograft tumors in vivo. Anticancer Drugs 21:186–192

    Article  PubMed  CAS  Google Scholar 

  • Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, Hernandez-Boussard T, Livasy C, Cowan D, Dressler L, Akslen LA, Ragaz J, Gown AM, Gilks CB, van de Rijn M, Perou CM (2004) Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 10:5367–5374

    Article  PubMed  CAS  Google Scholar 

  • Oh B, Park S, Pak JH, Kim I (2012) Downregulation of Mcl-1 by daunorubicin pretreatment reverses resistance of breast cancer cells to TNF-related apoptosis-inducing ligand. Biochem Biophys Res Commun 422:42–47

    Article  PubMed  CAS  Google Scholar 

  • Oka N, Nakahara S, Takenaka Y, Fukumori T, Hogan V, Kanayama HO, Yanagawa T, Raz A (2005) Galectin-3 inhibits tumor necrosis factor–related apoptosis-inducing ligand-induced apoptosis by activating Akt in human bladder carcinoma cells. Cancer Res 65:7546–7553

    PubMed  CAS  Google Scholar 

  • Oliver PG, Lobuglio AF, Zhou T, Forero A, Kim H, Zinn KR, Zhai G, Li Y, Lee CH, Buchsbaum DJ (2012) Effect of anti-DR5 and chemotherapy on basal-like breast cancer. Breast Cancer Res Treat 133:417–426

    Article  PubMed  CAS  Google Scholar 

  • Ooi LL, Zheng Y, Zhou H, Trivedi T, Conigrave AD, Seibel MJ, Dunstan CR (2010a) Vitamin D deficiency promotes growth of MCF-7 human breast cancer in a rodent model of osteosclerotic bone metastasis. Bone 47:795–803

    Article  PubMed  CAS  Google Scholar 

  • Ooi LL, Zhou H, Kalak R, Zheng Y, Conigrave AD, Seibel MJ, Dunstan CR (2010b) Vitamin D deficiency promotes human breast cancer growth in a murine model of bone metastasis. Cancer Res 70:1835–1844

    Article  PubMed  CAS  Google Scholar 

  • Phipps LE, Hino S, Muschel RJ (2011) Targeting cell spreading: a method of sensitizing metastatic tumor cells to TRAIL-induced apoptosis. Mol Cancer Res 9:249–258

    Article  PubMed  CAS  Google Scholar 

  • Piechocki MP, Wu GS, Jones RF, Jacob JB, Gibson H, Ethier SP, Abrams J, Yagita H, Venuprasad K, Wei WZ (2012) Induction of proapoptotic antibodies to triple-negative breast cancer by vaccination with TRAIL death receptor DR5 DNA. Int J Cancer (in press)

  • Piggott L, Omidvar N, Pérez SM, Eberl M, Clarkson RW (2011) Suppression of apoptosis inhibitor c-FLIP selectively eliminates breast cancer stem cell activity in response to the anti-cancer agent, TRAIL. Breast Cancer Res 13:R88

    Article  PubMed  CAS  Google Scholar 

  • Rahman M, Davis SR, Pumphrey JG, Bao J, Nau MM, Meltzer PS, Lipkowitz S (2009) TRAIL induces apoptosis in triple-negative breast cancer cells with a mesenchymal phenotype. Breast Cancer Res Treat 113:217–230

    Article  PubMed  Google Scholar 

  • Ren YG, Wagner KW, Knee DA, Aza-Blanc P, Nasoff M, Deveraux QL (2004) Differential regulation of the TRAIL death receptors DR4 and DR5 by the signal recognition particle. Mol Biol Cell 15:5064–5074

    Article  PubMed  CAS  Google Scholar 

  • Rossi C, Di Lena A, La Sorda R, Lattanzio R, Antolini L, Patassini C, Piantelli M, Alberti S (2008) Intestinal tumour chemoprevention with the antioxidant lipoic acid stimulates the growth of breast cancer. Eur J Cancer 44:2696–2704

    Article  PubMed  CAS  Google Scholar 

  • Sawant RR, Vaze OS, Wang T, D’Souza GG, Rockwell K, Gada K, Khaw BA, Torchilin VP (2012) Palmitoyl ascorbate liposomes and free ascorbic acid: comparison of anticancer therapeutic effects upon parenteral administration. Pharm Res 29:375–383

    Article  PubMed  CAS  Google Scholar 

  • Shankar E, Sivaprasad U, Basu A (2008) Protein kinase C epsilon confers resistance of MCF-7 cells to TRAIL by Akt-dependent activation of Hdm2 and downregulation of p53. Oncogene 27:3957–3966

    Article  PubMed  CAS  Google Scholar 

  • Shankar S, Davis R, Singh KP, Kurzrock R, Ross DD, Srivastava RK (2009) Suberoylanilide hydroxamic acid (Zolinza/vorinostat) sensitizes TRAIL-resistant breast cancer cells orthotopically implanted in BALB/c nude mice. Mol Cancer Ther 8:1596–1605

    Article  PubMed  CAS  Google Scholar 

  • Srivastava RK, Kurzrock R, Shankar S (2010) MS-275 sensitizes TRAIL-resistant breast cancer cells, inhibits angiogenesis and metastasis, and reverses epithelial-mesenchymal transition in vivo. Mol Cancer Ther 9:3254–3266

    Article  PubMed  CAS  Google Scholar 

  • Sun NF, Meng QY, Tian AL, Hu SY, Wang RH, Liu ZX, Xu L (2012) Nanoliposome-mediated FL/TRAIL double-gene therapy for colon cancer: in vitro and in vivo evaluation. Cancer Lett 315:69–77

    Article  PubMed  CAS  Google Scholar 

  • Swami S, Krishnan AV, Wang JY, Jensen K, Peng L, Albertelli MA, Feldman D (2011) Inhibitory effects of calcitriol on the growth of MCF-7 breast cancer xenografts in nude mice: selective modulation of aromatase expression in vivo. Horm Cancer 2:190–202

    Article  PubMed  CAS  Google Scholar 

  • Swami S, Krishnan AV, Wang JY, Jensen K, Horst R, Albertelli MA, Feldman D (2012) Dietary vitamin d3 and 1,25-dihydroxyvitamin d3 (calcitriol) exhibit equivalent anticancer activity in mouse xenograft models of breast and prostate cancer. Endocrinology 153:2576–2587

    Article  PubMed  CAS  Google Scholar 

  • Szafran AA, Folks K, Warram J, Chanda D, Wang D, Zinn KR (2009) Death receptor 5 agonist TRA8 in combination with the bisphosphonate zoledronic acid attenuated the growth of breast cancer metastasis. Cancer Biol Ther 8:1109–1116

    Article  PubMed  CAS  Google Scholar 

  • Tenev T, Bianchi K, Darding M, Broemer M, Langlais C, Wallberg F, Zachariou A, Lopez J, MacFarlane M, Cain K, Meier P (2011) The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell 43:432–448

    Article  PubMed  CAS  Google Scholar 

  • Tsai JY, Hung CM, Bai ST, Huang CH, Chen WC, Chung JG, Kuo SC, Way TD, Huang LJ (2010) Induction of apoptosis by HAC-Y6, a novel microtubule inhibitor, through activation of the death receptor 4 signaling pathway in human hepatocellular carcinoma cells. Oncol Rep 24:1169–1178

    PubMed  CAS  Google Scholar 

  • Wagner KW, Punnoose EA, Januario T, Lawrence DA, Pitti RM, Lancaster K, Lee D, von Goetz M, Yee SF, Totpal K, Huw L, Katta V, Cavet G, Hymowitz SG, Amler L, Ashkenazi A (2007) Death-receptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL. Nat Med 13:1070–1077

    Article  PubMed  CAS  Google Scholar 

  • Wang JY, Swami S, Krishnan AV, Feldman D (2012) Combination of calcitriol and dietary soy exhibits enhanced anticancer activity and increased hypercalcemic toxicity in a mouse xenograft model of prostate cancer. Prostate. doi:10.1002/pros.22516

  • Wheatley MA, Cochran MC, Eisenbrey JR, Oum KL (2012) Cellular signal transduction can be induced by TRAIL conjugated to microcapsules. J Biomed Mater Res A (in press)

  • Wilmet JP, Tastet C, Desruelles E, Ziental-Gelus N, Blanckaert V, Hondermarck H, Le Bourhis X (2011) Proteome changes induced by overexpression of the p75 neurotrophin receptor (p75NTR) in breast cancer cells. Int J Dev Biol 55:801–809

    Article  PubMed  Google Scholar 

  • Wirapati P, Sotiriou C, Kunkel S, Farmer P, Pradervand S, Haibe-Kains B, Desmedt C, Ignatiadis M, Sengstag T, Schütz F, Goldstein DR, Piccart M, Delorenzi M (2008) Meta-analysis of gene expression profiles in breast cancer: toward a unified understanding of breast cancer subtyping and prognosis signatures. Breast Cancer Res 10:R65

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Omene C, Karkoszka J, Bosland M, Eckard J, Klein CB, Frenkel K (2011) Caffeic acid phenethyl ester (CAPE), derived from a honeybee product propolis, exhibits a diversity of anti-tumor effects in pre-clinical models of human breast cancer. Cancer Lett 308:43–53

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Yin S, Banerjee S, Sarkar F, Reddy KB (2011) Enhanced anticancer effect of the combination of cisplatin and TRAIL in triple-negative breast tumor cells. Mol Cancer Ther 10:550–557

    Article  PubMed  CAS  Google Scholar 

  • Yan S, Qu X, Xu C, Zhu Z, Zhang L, Xu L, Song N, Teng Y, Liu Y (2012) Down-regulation of Cbl-b by bufalin results in up-regulation of DR4/DR5 and sensitization of TRAIL-induced apoptosis in breast cancer cells. J Cancer Res Clin Oncol 138:1279–1289

    Article  PubMed  CAS  Google Scholar 

  • Yerbes R, López-Rivas A (2012) Itch/AIP4-independent proteasomal degradation of cFLIP induced by the histone deacetylase inhibitor SAHA sensitizes breast tumour cells to TRAIL. Invest New Drugs 30:541–547

    Article  PubMed  CAS  Google Scholar 

  • Yin S, Xu L, Bandyopadhyay S, Sethi S, Reddy KB (2011) Cisplatin and TRAIL enhance breast cancer stem cell death. Int J Oncol 39:891–898

    PubMed  CAS  Google Scholar 

  • Yoshida T, Shiraishi T, Horinaka M, Wakada M, Sakai T (2007) Glycosylation modulates TRAIL-R1/death receptor 4 protein: different regulations of two pro-apoptotic receptors for TRAIL by tunicamycin. Oncol Rep 18:1239–1242

    PubMed  CAS  Google Scholar 

  • Yu W, Jia L, Park SK, Li J, Gopalan A, Simmons-Menchaca M, Sanders BG, Kline K (2009) Anticancer actions of natural and synthetic vitamin E forms: RRR-alpha-tocopherol blocks the anticancer actions of gamma-tocopherol. Mol Nutr Food Res 53:1573–1581

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Zhang B (2008) TRAIL resistance of breast cancer cells is associated with constitutive endocytosis of death receptors 4 and 5. Mol Cancer Res 6:1861–1871

    Article  PubMed  CAS  Google Scholar 

  • Zhou Z, Liu R, Chen C (2012) The WWP1 ubiquitin E3 ligase increases TRAIL resistance in breast cancer. Int J Cancer 130:1504–1510

    Article  PubMed  CAS  Google Scholar 

  • Zinonos I, Labrinidis A, Lee M, Liapis V, Hay S, Ponomarev V, Diamond P, Findlay DM, Zannettino AC, Evdokiou A (2011) Anticancer efficacy of Apo2L/TRAIL is retained in the presence of high and biologically active concentrations of osteoprotegerin in vivo. J Bone Miner Res 26:630–643

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Lab for Translational Oncology and Personalized Medicine, Rashid Latif Medical College (RLMC), 35 km Ferozepur Road, Lahore, Pakistan

    Ammad Ahmad Farooqi & Sundas Fayyaz

  2. IMBB, The University of Lahore, Lahore, Pakistan

    Sundas Fayyaz, Muhammed Javed Iqbal & Shahzad Bhatti

  3. Department of Surgery, University College of Medicine, Lahore, Pakistan

    Muhammad Tahir

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  1. Ammad Ahmad Farooqi
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  2. Sundas Fayyaz
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  3. Muhammad Tahir
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  4. Muhammed Javed Iqbal
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  5. Shahzad Bhatti
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Correspondence to Ammad Ahmad Farooqi.

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Farooqi, A.A., Fayyaz, S., Tahir, M. et al. Breast Cancer Proteome Takes More Than Two to Tango on TRAIL: Beat Them at Their Own Game. J Membrane Biol 245, 763–777 (2012). https://doi.org/10.1007/s00232-012-9490-y

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  • DOI: https://doi.org/10.1007/s00232-012-9490-y

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