miR-200c Targets a NF-κB Up-Regulated TrkB/NTF3 Autocrine Signaling Loop to Enhance Anoikis Sensitivity in Triple Negative Breast Cancer

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Howe, Erin N ^a,b,c   Cochrane, Dawn R ^b   Cittelly, Diana M ^b   Richer, Jennifer K ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA 200C; NEUROTROPHIN 3; TRANSCRIPTION FACTOR RELA;

ANOIKIS; ARTICLE; AUTOCRINE EFFECT; CANCER RESISTANCE; CELL SURVIVAL; CELL SUSPENSION; CONTROLLED STUDY; ENZYME INDUCTION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN TARGETING; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION;

ANOIKIS; APOPTOSIS; AUTOCRINE COMMUNICATION; BREAST NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEUROTROPHIN 3; NF-KAPPA B; RECEPTOR, TRKB; SIGNAL TRANSDUCTION;

EID: 84869801719     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049987     Document Type: Article

References (85)

1. Siegel R, Naishadham D, Jemal A, (2012) Cancer statistics, 2012. CA Cancer J Clin 62: 10-29 doi:10.3322/caac.20138.
2. Weigelt B, Peterse JL, van 't Veer LJ, (2005) Breast cancer metastasis: markers and models. Nat Rev Cancer 5: 591-602 doi:10.1038/nrc1670.
3. Drasin DJ, Robin TP, Ford HL, (2011) Breast cancer epithelial-to-mesenchymal transition: examining the functional consequences of plasticity. Breast Cancer Res 13: 226 doi:10.1186/bcr3037.
4. Pillai RS, Bhattacharyya SN, Filipowicz W, (2007) Repression of protein synthesis by miRNAs: how many mechanisms? Trends in Cell Biology 17: 118-126.
5. Bartel DP, (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
6. Cochrane DR, Cittelly DM, Howe EN, Spoelstra NS, McKinsey EL, et al. (2010) MicroRNAs link estrogen receptor alpha status and Dicer levels in breast cancer. Horm Cancer 1: 306-319 doi:10.1007/s12672-010-0043-5.
7. Stinson S, Lackner MR, Adai AT, Yu N, Kim H-J, et al. (2011) miR-221/222 targeting of trichorhinophalangeal 1 (TRPS1) promotes epithelial-to-mesenchymal transition in breast cancer. Sci Signal 4: pt5 doi:10.1126/scisignal.2002258.
8. Hurteau GJ, Carlson JA, Spivack SD, Brock GJ, (2007) Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Research 67: 7972-7976.
9. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, et al. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nature Cell Biology 10: 593-601.
10. Park S-M, Gaur AB, Lengyel E, Peter ME, (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes & Development 22: 894-907.
11. Howe EN, Cochrane DR, Richer JK, (2011) Targets of miR-200c mediate suppression of cell motility and anoikis resistance. Breast Cancer Res 13: R45 doi:10.1186/bcr2867.
12. Sossey-Alaoui K, Bialkowska K, Plow EF, (2009) The miR200 family of microRNAs regulates WAVE3-dependent cancer cell invasion. The Journal of Biological Chemistry 284: 33019-33029.
13. Eades G, Yao Y, Yang M, Zhang Y, Chumsri S, et al. (2011) miR-200a regulates SIRT1 expression and epithelial to mesenchymal transition (EMT)-like transformation in mammary epithelial cells. J Biol Chem 286: 25992-26002 doi:10.1074/jbc.M111.229401.
14. Iliopoulos D, Lindahl-Allen M, Polytarchou C, Hirsch HA, Tsichlis PN, et al. (2010) Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol Cell 39: 761-772 doi:10.1016/j.molcel.2010.08.013.
15. Meredith JE Jr, Fazeli B, Schwartz MA, (1993) The extracellular matrix as a cell survival factor. Mol Biol Cell 4: 953-961.
16. Frisch SM, Francis H, (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124: 619-626.
17. Horbinski C, Mojesky C, Kyprianou N, (2010) Live free or die: tales of homeless (cells) in cancer. Am J Pathol 177: 1044-1052 doi:10.2353/ajpath.2010.091270.
18. Coates JM, Galante JM, Bold RJ, (2010) Cancer therapy beyond apoptosis: autophagy and anoikis as mechanisms of cell death. J Surg Res 164: 301-308 doi:10.1016/j.jss.2009.07.011.
19. Geiger TR, Peeper DS, (2009) Metastasis mechanisms. Biochim Biophys Acta 1796: 293-308 doi:10.1016/j.bbcan.2009.07.006.
20. Klymkowsky MW, Savagner P, (2009) Epithelial-mesenchymal transition: a cancer researcher's conceptual friend and foe. Am J Pathol 174: 1588-1593 doi:10.2353/ajpath.2009.080545.
21. Smit MA, Geiger TR, Song J-Y, Gitelman I, Peeper DS, (2009) A Twist-Snail axis critical for TrkB-induced epithelial-mesenchymal transition-like transformation, anoikis resistance, and metastasis. Molecular and Cellular Biology 29: 3722-3737.
22. Smit MA, Peeper DS, (2011) Zeb1 is required for TrkB-induced epithelial-mesenchymal transition, anoikis resistance and metastasis. Oncogene 30: 3735-3744 doi:10.1038/onc.2011.96.
23. Grooteclaes ML, Frisch SM, (2000) Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene 19: 3823-3828 doi:10.1038/sj.onc.1203721.
24. Kumar S, Park SH, Cieply B, Schupp J, Killiam E, et al. (2011) A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol Cell Biol 31: 4036-4051 doi:10.1128/MCB.01342-10.
25. Klein R, (1994) Role of neurotrophins in mouse neuronal development. FASEB J 8: 738-744.
26. Ernsberger U, (2009) Role of neurotrophin signalling in the differentiation of neurons from dorsal root ganglia and sympathetic ganglia. Cell Tissue Res 336: 349-384 doi:10.1007/s00441-009-0784-z.
27. Stoilov P, Castren E, Stamm S, (2002) Analysis of the human TrkB gene genomic organization reveals novel TrkB isoforms, unusual gene length, and splicing mechanism. Biochemical and Biophysical Research Communications 290: 1054-1065.
28. Douma S, Van Laar T, Zevenhoven J, Meuwissen R, Van Garderen E, et al. (2004) Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB. Nature 430: 1034-1039.
29. Geiger TR, Peeper DS, (2007) Critical role for TrkB kinase function in anoikis suppression, tumorigenesis, and metastasis. Cancer Research 67: 6221-6229.
30. Yu X, Liu L, Cai B, He Y, Wan ×, (2008) Suppression of anoikis by the neurotrophic receptor TrkB in human ovarian cancer. Cancer Science 99: 543-552.
31. Siu MKY, Wong OGW, Cheung ANY, (2009) TrkB as a therapeutic target for ovarian cancer. Expert Opinion on Therapeutic Targets 13: 1169-1178.
32. Kupferman ME, Jiffar T, El-Naggar A, Yilmaz T, Zhou G, et al. (2010) TrkB induces EMT and has a key role in invasion of head and neck squamous cell carcinoma. Oncogene 29: 2047-2059.
33. Sadick MD, Galloway A, Shelton D, Hale V, Weck S, et al. (1997) Analysis of neurotrophin/receptor interactions with a gD-flag-modified quantitative kinase receptor activation (gD.KIRA) enzyme-linked immunosorbent assay. Exp Cell Res 234: 354-361 doi:10.1006/excr.1997.3614.
34. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, et al. (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10: 515-527 doi:10.1016/j.ccr.2006.10.008.
35. Nakagawara A, (2001) Trk receptor tyrosine kinases: a bridge between cancer and neural development. Cancer Lett 169: 107-114.
36. Thompson EW, Newgreen DF, Tarin D (2005) Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition? Cancer Res 65: 5991-5995; discussion 5995. doi:10.1158/0008-5472.CAN-05-0616.
37. Zanotti S, Gibertini S, Bragato C, Mantegazza R, Morandi L, et al. (2011) Fibroblasts from the muscles of Duchenne muscular dystrophy patients are resistant to cell detachment apoptosis. Exp Cell Res 317: 2536-2547 doi:10.1016/j.yexcr.2011.08.004.
38. Giannoni E, Buricchi F, Grimaldi G, Parri M, Cialdai F, et al. (2008) Redox regulation of anoikis: reactive oxygen species as essential mediators of cell survival. Cell Death Differ 15: 867-878 doi:10.1038/cdd.2008.3.
39. Ilić D, Almeida EA, Schlaepfer DD, Dazin P, Aizawa S, et al. (1998) Extracellular matrix survival signals transduced by focal adhesion kinase suppress p53-mediated apoptosis. J Cell Biol 143: 547-560.
40. Almeida EA, Ilić D, Han Q, Hauck CR, Jin F, et al. (2000) Matrix survival signaling: from fibronectin via focal adhesion kinase to c-Jun NH(2)-terminal kinase. J Cell Biol 149: 741-754.
41. Gregory PA, Bracken CP, Bert AG, Goodall GJ, (2008) MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle 7: 3112-3118.
42. Wright JA, Richer JK, Goodall GJ, (2010) microRNAs and EMT in mammary cells and breast cancer. J Mammary Gland Biol Neoplasia 15: 213-223 doi:10.1007/s10911-010-9183-z.
43. Howe EN, Cochrane DR, Richer JK (2012) The miR-200 and miR-221/222 microRNA Families: Opposing Effects on Epithelial Identity. Journal of Mammary Gland Biology and Neoplasia. Available:http://www.ncbi.nlm.nih.gov/pubmed/22350980. Accessed 28 February 2012.
44. Chiarugi P, Giannoni E, (2008) Anoikis: a necessary death program for anchorage-dependent cells. Biochem Pharmacol 76: 1352-1364 doi:10.1016/j.bcp.2008.07.023.
45. Taddei ML, Giannoni E, Fiaschi T, Chiarugi P, (2012) Anoikis: an emerging hallmark in health and diseases. J Pathol 226: 380-393 doi:10.1002/path.3000.
46. Gramantieri L, Fornari F, Ferracin M, Veronese A, Sabbioni S, et al. (2009) MicroRNA-221 targets Bmf in hepatocellular carcinoma and correlates with tumor multifocality. Clin Cancer Res 15: 5073-5081 doi:10.1158/1078-0432.CCR-09-0092.
47. Penna E, Orso F, Cimino D, Tenaglia E, Lembo A, et al. (2011) microRNA-214 contributes to melanoma tumour progression through suppression of TFAP2C. EMBO J 30: 1990-2007 doi:10.1038/emboj.2011.102.
48. Wang X, Tian L-L, Jiang X-Y, Wang Y-Y, Li D-G, et al. (2011) The expression and function of miRNA-451 in non-small cell lung cancer. Cancer Lett 311: 203-209 doi:10.1016/j.canlet.2011.07.026.
49. Lv X-B, Jiao Y, Qing Y, Hu H, Cui X, et al. (2011) miR-124 suppresses multiple steps of breast cancer metastasis by targeting a cohort of pro-metastatic genes in vitro. Chin J Cancer 30: 821-830 doi:10.5732/cjc.011.10289.
50. Huang YT, Lai PC, Wu CC, Hsu SH, Cheng CC, et al. (2010) BDNF mediated TrkB activation is a survival signal for transitional cell carcinoma cells. Int J Oncol 36: 1469-1476.
51. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, et al. (2008) A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68: 7846-7854 doi:10.1158/0008-5472.CAN-08-1942.
52. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, et al. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Reports 9: 582-589.
53. Cieply B, Riley P 4th, Pifer PM, Widmeyer J, Addison JB, et al (2012) Suppression of the epithelial-mesenchymal transition by Grainyhead-like-2. Cancer Res 72: 2440-2453 doi:10.1158/0008-5472.CAN-11-4038.
54. Ghosh S, May MJ, Kopp EB, (1998) NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16: 225-260 doi:10.1146/annurev.immunol.16.1.225.
55. Fusco AJ, Huang D-B, Miller D, Wang VY-F, Vu D, et al. (2009) NF-kappaB p52:RelB heterodimer recognizes two classes of kappaB sites with two distinct modes. EMBO Rep 10: 152-159 doi:10.1038/embor.2008.227.
56. Häcker H, Karin M, (2006) Regulation and function of IKK and IKK-related kinases. Sci STKE 2006: re13 doi:10.1126/stke.3572006re13.
57. Oeckinghaus A, Ghosh S, (2009) The NF-kappaB family of transcription factors and its regulation. Cold Spring Harb Perspect Biol 1: a000034 doi:10.1101/cshperspect.a000034.
58. Mantovani A, Marchesi F, Portal C, Allavena P, Sica A, (2008) Linking inflammation reactions to cancer: novel targets for therapeutic strategies. Adv Exp Med Biol 610: 112-127.
59. Dev A, Iyer S, Razani B, Cheng G, (2011) NF-κB and innate immunity. Curr Top Microbiol Immunol 349: 115-143 doi:10.1007/82_2010_102.
60. Sen R, Baltimore D, (1986) Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46: 705-716.
61. Escárcega RO, Fuentes-Alexandro S, García-Carrasco M, Gatica A, Zamora A, (2007) The transcription factor nuclear factor-kappa B and cancer. Clin Oncol (R Coll Radiol) 19: 154-161.
62. Ben-Neriah Y, Karin M, (2011) Inflammation meets cancer, with NF-κB as the matchmaker. Nat Immunol 12: 715-723 doi:10.1038/ni.2060.
63. Creedon DJ, Johnson EM, Lawrence JC, (1996) Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J Biol Chem 271: 20713-20718.
64. Crowder RJ, Freeman RS, (1998) Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J Neurosci 18: 2933-2943.
65. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, et al. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275: 661-665.
66. Jin W, Kim GM, Kim MS, Lim MH, Yun C, et al. (2010) TrkC plays an essential role in breast tumor growth and metastasis. Carcinogenesis 31: 1939-1947 doi:10.1093/carcin/bgq180.
67. Lin D-C, Zhang Y, Pan Q-J, Yang H, Shi Z-Z, et al. (2011) PLK1 Is Transcriptionally Activated by NF-{kappa}B during Cell Detachment and Enhances Anoikis Resistance through Inhibiting {beta}-Catenin Degradation in Esophageal Squamous Cell Carcinoma. Clin Cancer Res. Available:http://www.ncbi.nlm.nih.gov/pubmed/21610149. Accessed 6 July 2011.
68. Yu X, Cohen DM, Chen CS (2012) miR-125b is an Adhesion-Regulated microRNA that Protects Mesenchymal Stem Cells from Anoikis. Stem Cells (Dayton, Ohio). Available:http://www.ncbi.nlm.nih.gov/pubmed/22331826. Accessed 28 February 2012.
69. Campbell ID, Humphries MJ (2011) Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol 3. Available:http://www.ncbi.nlm.nih.gov/pubmed/21421922. Accessed 1 March 2012.
70. Saldanha-Gama RF, Moraes JA, Mariano-Oliveira A, Coelho AL, Walsh EM, et al. (2010) alpha(9)beta(1) integrin engagement inhibits neutrophil spontaneous apoptosis: involvement of Bcl-2 family members. Biochim Biophys Acta 1803: 848-857 doi:10.1016/j.bbamcr.2010.03.012.
71. Antonov AS, Antonova GN, Munn DH, Mivechi N, Lucas R, et al. (2011) αVβ3 integrin regulates macrophage inflammatory responses via PI3 kinase/Akt-dependent NF-κB activation. J Cell Physiol 226: 469-476 doi:10.1002/jcp.22356.
72. Neri P, Ren L, Azab AK, Brentnall M, Gratton K, et al. (2011) Integrin β7-mediated regulation of multiple myeloma cell adhesion, migration, and invasion. Blood 117: 6202-6213 doi:10.1182/blood-2010-06-292243.
73. Bhatia V, Mula RV, Weigel NL, Falzon M, (2009) Parathyroid hormone-related protein regulates cell survival pathways via integrin alpha6beta4-mediated activation of phosphatidylinositol 3-kinase/Akt signaling. Mol Cancer Res 7: 1119-1131 doi:10.1158/1541-7786.MCR-08-0568.
74. Prakash M, Kale S, Ghosh I, Kundu GC, Datta K, (2011) Hyaluronan-binding protein 1 (HABP1/p32/gC1qR) induces melanoma cell migration and tumor growth by NF-kappa B dependent MMP-2 activation through integrin α(v)β(3) interaction. Cell Signal 23: 1563-1577 doi:10.1016/j.cellsig.2011.04.009.
75. Shih Y-W, Chien S-T, Chen P-S, Lee J-H, Wu S-H, et al. (2010) Alpha-mangostin suppresses phorbol 12-myristate 13-acetate-induced MMP-2/MMP-9 expressions via alphavbeta3 integrin/FAK/ERK and NF-kappaB signaling pathway in human lung adenocarcinoma A549 cells. Cell Biochem Biophys 58: 31-44 doi:10.1007/s12013-010-9091-2.
76. Dia VP, Gonzalez de Mejia E, (2011) Lunasin potentiates the effect of oxaliplatin preventing outgrowth of colon cancer metastasis, binds to α5β1 integrin and suppresses FAK/ERK/NF-κB signaling. Cancer Lett 313: 167-180 doi:10.1016/j.canlet.2011.09.002.
77. Mino K, Ozaki M, Nakanishi K, Haga S, Sato M, et al. (2011) Inhibition of nuclear factor-kappaB suppresses peritoneal dissemination of gastric cancer by blocking cancer cell adhesion. Cancer Sci 102: 1052-1058 doi:10.1111/j.1349-7006.2011.01901.x.
78. Hyun S, Lee JH, Jin H, Nam J, Namkoong B, et al. (2009) Conserved MicroRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 139: 1096-1108 doi:10.1016/j.cell.2009.11.020.
79. Xia W, Li J, Chen L, Huang B, Li S, et al. (2010) MicroRNA-200b regulates cyclin D1 expression and promotes S-phase entry by targeting RND3 in HeLa cells. Mol Cell Biochem 344: 261-266 doi:10.1007/s11010-010-0550-2.
80. Cochrane DR, Spoelstra NS, Howe EN, Nordeen SK, Richer JK (2009) MicroRNA-200c mitigates invasiveness and restores sensitivity to microtubule-targeting chemotherapeutic agents. Molecular Cancer Therapeutics. Available:http://www.ncbi.nlm.nih.gov/pubmed/19435871.
81. Cochrane DR, Howe EN, Spoelstra NS, Richer JK, (2010) Loss of miR-200c: A Marker of Aggressiveness and Chemoresistance in Female Reproductive Cancers. Journal of Oncology 2010: 821717.
82. Chen J, Tian W, Cai H, He H, Deng Y (2011) Down-regulation of microRNA-200c is associated with drug resistance in human breast cancer. Medical Oncology (Northwood, London, England). Available:http://www.ncbi.nlm.nih.gov/pubmed/22101791. Accessed 12 December 2011.
83. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, et al. (2009) Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 138: 592-603.
84. Kuramoto H, Nishida M, Morisawa T, Hamano M, Hata H, et al. (1991) Establishment and characterization of human endometrial cancer cell lines. Ann N Y Acad Sci 622: 402-421.
85. Nelson JD, Denisenko O, Bomsztyk K, (2006) Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat Protoc 1: 179-185 doi:10.1038/nprot.2006.27.