Advertisement

The Journal of Membrane Biology

, Volume 245, Issue 12, pp 763–777 | Cite as

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

  • Ammad Ahmad Farooqi
  • Sundas Fayyaz
  • Muhammad Tahir
  • Muhammed Javed Iqbal
  • Shahzad Bhatti
Topical Review

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.

Keywords

Biochemistry/molecular biology Cell physiology Cell signaling Membrane transport Membrane-drug physical interaction Structure function membrane rafts Transport physiology 

References

  1. 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 11:1518–1527PubMedCrossRefGoogle Scholar
  2. Amm HM, Buchsbaum DJ (2011) Relationship between galectin-3 expression and TRAIL sensitivity in breast cancer. Expert Rev Anticancer Ther 11:1193–1196PubMedCrossRefGoogle Scholar
  3. 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 9:403–417PubMedCrossRefGoogle Scholar
  4. 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 103:10283–10288PubMedCrossRefGoogle Scholar
  5. 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 33:1536–1546PubMedCrossRefGoogle Scholar
  6. Bolanz KA, Hediger MA, Landowski CP (2008) The role of TRPV6 in breast carcinogenesis. Mol Cancer Ther 7:271–279PubMedCrossRefGoogle Scholar
  7. 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 7:2000–2010PubMedCrossRefGoogle Scholar
  8. Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447PubMedCrossRefGoogle Scholar
  9. 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 20:538–549PubMedCrossRefGoogle Scholar
  10. 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 10:212PubMedCrossRefGoogle Scholar
  11. 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 28:813–822PubMedCrossRefGoogle Scholar
  12. 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 6:1991–2005Google Scholar
  13. 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 287:641–649PubMedCrossRefGoogle Scholar
  14. 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 16:394–403PubMedCrossRefGoogle Scholar
  15. 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 131:1052–1058PubMedCrossRefGoogle Scholar
  16. 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 17:1435–1447PubMedCrossRefGoogle Scholar
  17. 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 23:335–346PubMedCrossRefGoogle Scholar
  18. 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 9:263PubMedCrossRefGoogle Scholar
  19. 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 23:426–436PubMedCrossRefGoogle Scholar
  20. 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 33:1428–1436PubMedCrossRefGoogle Scholar
  21. 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 63:773–787PubMedCrossRefGoogle Scholar
  22. 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 31:200–212PubMedCrossRefGoogle Scholar
  23. Ganai S, Arenas RB, Forbes NS (2009) Tumour-targeted delivery of TRAIL using Salmonella typhimurium enhances breast cancer survival in mice. Br J Cancer 101:1683–1691PubMedCrossRefGoogle Scholar
  24. 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 152:84–89PubMedCrossRefGoogle Scholar
  25. Garimella SV, Rocca A, Lipkowitz S (2012) WEE1 inhibition sensitizes basal breast cancer cells to TRAIL-induced apoptosis. Mol Cancer Res 10:75–85PubMedCrossRefGoogle Scholar
  26. 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) 73:358–362CrossRefGoogle Scholar
  27. 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 70:3718–3729PubMedCrossRefGoogle Scholar
  28. 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 8:125PubMedCrossRefGoogle Scholar
  29. 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–C502PubMedCrossRefGoogle Scholar
  30. 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 27:441–446PubMedGoogle Scholar
  31. Hafid SR, Radhakrishnan AK, Nesaretnam K (2010) Tocotrienols are good adjuvants for developing cancer vaccines. BMC Cancer 10:5PubMedCrossRefGoogle Scholar
  32. 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 8:1570–1578PubMedCrossRefGoogle Scholar
  33. 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 11:471PubMedCrossRefGoogle Scholar
  34. 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 32:1242–1252PubMedCrossRefGoogle Scholar
  35. 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 9:539–550PubMedCrossRefGoogle Scholar
  36. 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 138:2357–2367PubMedCrossRefGoogle Scholar
  37. 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 33:851–859PubMedGoogle Scholar
  38. 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) 3:993–1002CrossRefGoogle Scholar
  39. 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 9:262PubMedCrossRefGoogle Scholar
  40. 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 63:471–482PubMedCrossRefGoogle Scholar
  41. 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 279:35829–35839PubMedCrossRefGoogle Scholar
  42. 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 134:139–155PubMedCrossRefGoogle Scholar
  43. 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 72:2057–2067PubMedCrossRefGoogle Scholar
  44. 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 68:3440–3449PubMedCrossRefGoogle Scholar
  45. 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 1812:796–805PubMedCrossRefGoogle Scholar
  46. 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 100:482–491PubMedCrossRefGoogle Scholar
  47. 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 138:1155–1163PubMedCrossRefGoogle Scholar
  48. Kohlhaas SL, Craxton A, Sun XM, Pinkoski MJ, Cohen GM (2007) Receptor-mediated endocytosis is not required for TRAIL-induced apoptosis. J Biol Chem 282:12831–12841PubMedCrossRefGoogle Scholar
  49. 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 27:1472–1477PubMedCrossRefGoogle Scholar
  50. 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 31:805–817PubMedCrossRefGoogle Scholar
  51. Landowski CP, Bolanz KA, Suzuki Y, Hediger MA (2011) Chemical inhibitors of the calcium entry channel TRPV6. Pharm Res 28:322–330PubMedCrossRefGoogle Scholar
  52. 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) 234:1244–1252CrossRefGoogle Scholar
  53. 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 288:21–34PubMedCrossRefGoogle Scholar
  54. 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 59:1073–1081PubMedCrossRefGoogle Scholar
  55. 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 7:1512–1522PubMedCrossRefGoogle Scholar
  56. 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 11:296–307PubMedCrossRefGoogle Scholar
  57. Leong S, McKay MJ, Christopherson RI, Baxter RC (2012) Biomarkers of breast cancer apoptosis induced by chemotherapy and TRAIL. J Proteome Res 11:1240–1250PubMedCrossRefGoogle Scholar
  58. 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 61:1255–1268PubMedCrossRefGoogle Scholar
  59. 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 32:3538–3546PubMedCrossRefGoogle Scholar
  60. 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 379:626–631PubMedCrossRefGoogle Scholar
  61. 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 32:154–167PubMedCrossRefGoogle Scholar
  62. 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 47:1890–1907PubMedCrossRefGoogle Scholar
  63. 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 90:612–618PubMedCrossRefGoogle Scholar
  64. 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 12:153CrossRefGoogle Scholar
  65. 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 133:437–445PubMedCrossRefGoogle Scholar
  66. 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 10:902–914PubMedCrossRefGoogle Scholar
  67. 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 104:281–289PubMedCrossRefGoogle Scholar
  68. 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 17:5005–5015PubMedCrossRefGoogle Scholar
  69. 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 282:21337–21348PubMedCrossRefGoogle Scholar
  70. 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 117:4375–4380PubMedCrossRefGoogle Scholar
  71. 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 19:523–533PubMedCrossRefGoogle Scholar
  72. 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:e20920PubMedCrossRefGoogle Scholar
  73. 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
  74. 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) 90:309–319CrossRefGoogle Scholar
  75. 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 21:186–192PubMedCrossRefGoogle Scholar
  76. 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 10:5367–5374PubMedCrossRefGoogle Scholar
  77. 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 422:42–47PubMedCrossRefGoogle Scholar
  78. 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 65:7546–7553PubMedGoogle Scholar
  79. 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 133:417–426PubMedCrossRefGoogle Scholar
  80. 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 47:795–803PubMedCrossRefGoogle Scholar
  81. 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 70:1835–1844PubMedCrossRefGoogle Scholar
  82. Phipps LE, Hino S, Muschel RJ (2011) Targeting cell spreading: a method of sensitizing metastatic tumor cells to TRAIL-induced apoptosis. Mol Cancer Res 9:249–258PubMedCrossRefGoogle Scholar
  83. 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)Google Scholar
  84. 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:R88PubMedCrossRefGoogle Scholar
  85. 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 113:217–230PubMedCrossRefGoogle Scholar
  86. 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 15:5064–5074PubMedCrossRefGoogle Scholar
  87. 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 44:2696–2704PubMedCrossRefGoogle Scholar
  88. 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 29:375–383PubMedCrossRefGoogle Scholar
  89. 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 27:3957–3966PubMedCrossRefGoogle Scholar
  90. 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 8:1596–1605PubMedCrossRefGoogle Scholar
  91. 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 9:3254–3266PubMedCrossRefGoogle Scholar
  92. 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 315:69–77PubMedCrossRefGoogle Scholar
  93. 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 2:190–202PubMedCrossRefGoogle Scholar
  94. 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 153:2576–2587PubMedCrossRefGoogle Scholar
  95. 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 8:1109–1116PubMedCrossRefGoogle Scholar
  96. 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 43:432–448PubMedCrossRefGoogle Scholar
  97. 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 24:1169–1178PubMedGoogle Scholar
  98. 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 13:1070–1077PubMedCrossRefGoogle Scholar
  99. 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
  100. 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)Google Scholar
  101. 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 55:801–809PubMedCrossRefGoogle Scholar
  102. 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:R65PubMedCrossRefGoogle Scholar
  103. 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 308:43–53PubMedCrossRefGoogle Scholar
  104. 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 10:550–557PubMedCrossRefGoogle Scholar
  105. 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 138:1279–1289PubMedCrossRefGoogle Scholar
  106. 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 30:541–547PubMedCrossRefGoogle Scholar
  107. Yin S, Xu L, Bandyopadhyay S, Sethi S, Reddy KB (2011) Cisplatin and TRAIL enhance breast cancer stem cell death. Int J Oncol 39:891–898PubMedGoogle Scholar
  108. 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 18:1239–1242PubMedGoogle Scholar
  109. 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 53:1573–1581PubMedCrossRefGoogle Scholar
  110. 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 6:1861–1871PubMedCrossRefGoogle Scholar
  111. Zhou Z, Liu R, Chen C (2012) The WWP1 ubiquitin E3 ligase increases TRAIL resistance in breast cancer. Int J Cancer 130:1504–1510PubMedCrossRefGoogle Scholar
  112. 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 26:630–643PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Ammad Ahmad Farooqi
    • 1
  • Sundas Fayyaz
    • 1
    • 2
  • Muhammad Tahir
    • 3
  • Muhammed Javed Iqbal
    • 2
  • Shahzad Bhatti
    • 2
  1. 1.Lab for Translational Oncology and Personalized MedicineRashid Latif Medical College (RLMC)LahorePakistan
  2. 2.IMBBThe University of LahoreLahorePakistan
  3. 3.Department of SurgeryUniversity College of MedicineLahorePakistan

Personalised recommendations