TGFβ-induced c-Myb affects the expression of EMT-associated genes and promotes invasion of ER+ breast cancer cells

Cell Cycle

Volumn 10, Issue 23, 2011, Pages 4149-4161

  Cesi, Vincenzo ^a   Casciati, Arianna ^a   Sesti, Fabiola ^a   Tanno, Barbara ^a   Calabretta, Bruno ^b   Raschellà, Giuseppe ^a  

^a ENEA C R CASACCIA   (Italy)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Apoptosis; Breast cancer; c Myb; EMT; Invasion; MiRNA; SiRNA; TGF

Indexed keywords

ESTROGEN RECEPTOR; ETOPOSIDE; LUCIFERASE; MICRORNA; MICRORNA 200B; MICRORNA 200C; MICRORNA 429; PROTEIN BCL 2; PROTEIN C MYB; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG; UVOMORULIN;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER INVASION; CELL ANCHORAGE; CELL COUNT; CELL GROWTH; CELL INVASION; CELL STRAIN MCF 7; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE MAPPING; GENE SILENCING; GENE VECTOR; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HALF LIFE TIME; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; RNA BINDING;

EID: 82855170853     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.23.18346     Document Type: Article

References (92)

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28. Guérin M, Sheng ZM, Andrieu N, Riou G. Strong association between c-myb and oestrogen-receptor expression in human breast cancer. Oncogene 1990; 5:131-5; PMID:2181374.
29. Salomoni P, Perrotti D, Martinez R, Franceschi C, Calabretta B. Resistance to apoptosis in CTLL-2 cells constitutively expressing c-Myb is associated with induction of BCL-2 expression and Myb-dependent regulation of bcl-2 promoter activity. Proc Natl Acad Sci USA 1997; 94:3296-301;PMID:9096387; DOI:10.1073/pnas.94.7.3296.
30. Zhang M, Zhang Z, Pan HY, Wang DX, Deng ZT, Ye XL. TGFbeta1 induces human bronchial epithelial cell-to-mesenchymal transition in vitro. Lung 2009; 187:187-94;PMID:19252942; DOI:10.1007/s00408-009-9139-5.
31. Wieser R, Wrana JL, Massague J. GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGFbeta receptor complex. EMBO J 1995; 14:2199-208; PMID:7774578.
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42. Yang L, Pang Y, Moses HL. TGFbeta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol 2010; 31:220-7;PMID:20538542; DOI:10.1016/j.it.2010.04.002.
43. Kanzaki S, Hilliker S, Baylink DJ, Mohan S. Evidence that human bone cells in culture produce insulin-like growth factor-binding protein-4 and -5 proteases. Endocrinology 1994; 134:383-92;PMID:7506211; DOI:10.1210/en.134.1. 383.
44. Lüscher B, Eisenman RN. c-myc and c-myb protein degradation: effect of metabolic inhibitors and heat shock. Mol Cell Biol 1988; 8:2504-12; PMID:3043180.
45. McNeill RE, Miller N, Kerin MJ. Evaluation and validation of candidate endogenous control genes for real-time quantitative PCR studies of breast cancer. BMC Mol Biol 2007; 8:107;PMID:18042273; DOI:10.1186/1471-2199-8-107.
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49. Shi Y, Massague J. Mechanisms of TGFbeta signaling from cell membrane to the nucleus. Cell 2003; 113:685-700;PMID:12809600; DOI:10.1016/ S0092-8674(03)00432-X.
50. Gomis RR, Alarcon C, He W, Wang Q, Seoane J, Lash A, et al. A FoxO-Smad synexpression group in human keratinocytes. Proc Natl Acad Sci USA 2006; 103:12747-52;PMID:16908841; DOI:10.1073/ pnas.0605333103.
51. Lu T, Tian L, Han Y, Vogelbaum M, Stark GR. Dose-dependent cross-talk between the transforming growth factorbeta and interleukin-1 signaling pathways. Proc Natl Acad Sci USA 2007; 104:4365-70;PMID:17360530; DOI:10.1073/pnas. 0700118104.
52. Juárez P, Guise TA. TGFβ in cancer and bone: implications for treatment of bone metastases. Bone 2011; 48:23-9;PMID:20699127; DOI:10.1016/j. bone.2010.08.004.
53. Levy L, Hill CS. Alterations in components of the TGFbeta superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev 2006; 17:41- 58;PMID:16310402; DOI:10.1016/j.cytogfr. 2005.09.009.
54. Cerutti JM, Ebina KN, Matsuo SE, Martins L, Maciel RM, Kimura ET. Expression of Smad4 and Smad7 in human thyroid follicular carcinoma cell lines. J Endocrinol Invest 2003; 26:516-21; PMID:12952364.
55. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139:871-90;PMID:19945376; DOI:10.1016/j.cell.2009.11.007.
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59. Nam JS, Terabe M, Kang MJ, Chae H, Voong N, Yang YA, et al. Transforming growth factorbeta subverts the immune system into directly promoting tumor growth through interleukin-17. Cancer Res 2008; 68:3915-23;PMID:18483277; DOI:10.1158/0008-5472.CAN- 08-0206.
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61. Malhotra GK, Zhao X, Band H, Band V. Histological, molecular and functional subtypes of breast cancers. Cancer Biol Ther 2010; 10:955-60;PMID:21057215; DOI:10.4161/cbt.10.10.13879.
62. Prat A, Perou CM. Deconstructing the molecular portraits of breast cancer. Mol Oncol 2011; 5:5-23;PMID:21147047; DOI:10.1016/j. molonc.2010.11.003.
63. Parvani JG, Taylor MA, Schiemann WP. Noncanonical TGFbeta Signaling During Mammary Tumorigenesis. J Mammary Gland Biol Neoplasia 2011; 16:127-46;PMID:21448580; DOI:10.1007/s10911-011-9207-3.
64. Serra R, Crowley MR. TGFbeta in mammary gland development and breast cancer. Breast Dis 2003; 18:61-73; PMID:15687689.
65. Chen T, Carter D, Garrigue-Antar L, Reiss M. Transforming growth factorbeta type I receptor kinase mutant associated with metastatic breast cancer. Cancer Res 1998; 58:4805-10; PMID:9809982.
66. Albini A, Sporn MB. The tumour microenvironment as a target for chemoprevention. Nat Rev Cancer 2007; 7:139-47;PMID:17218951; DOI:10.1038/nrc2067.
67. Ramsay RG, Gonda TJ. MYB function in normal and cancer cells. Nat Rev Cancer 2008; 8:523-34;PMID:18574464; DOI:10.1038/nrc2439.
68. Anfossi G, Gewirtz AM, Calabretta B. An oligomer complementary to c-myb-encoded mRNA inhibits proliferation of human myeloid leukemia cell lines. Proc Natl Acad Sci USA 1989; 86:3379-83;PMID:2541445; DOI:10.1073/pnas.86.9. 3379.
69. Clappier E, Cuccuini W, Kalota A, Crinquette A, Cayuela JM, Dik WA, et al. The C-MYB locus is involved in chromosomal translocation and genomic duplications in human T-cell acute leukemia (T-ALL), the translocation defining a new T-ALL subtype in very young children. Blood 2007; 110:1251-61;PMID: 17452517; DOI:10.1182/blood-2006-12- 064683.
70. Drabsch Y, Hugo H, Zhang R, Dowhan DH, Miao YR, Gewirtz AM, et al. Mechanism of and requirement for estrogen-regulated MYB expression in estrogen-receptor- positive breast cancer cells. Proc Natl Acad Sci USA 2007; 104:13762-7;PMID:17690249; DOI:10.1073/ pnas.0700104104.
71. Hugo H, Cures A, Suraweera N, Drabsch Y, Purcell D, Mantamadiotis T, et al. Mutations in the MYB intron I regulatory sequence increase transcription in colon cancers. Genes Chromosomes Cancer 2006; 45:1143- 54;PMID:16977606; DOI:10.1002/gcc.20378.
72. Tanno B, Sesti F, Cesi V, Bossi G, Ferrari-Amorotti G, Bussolari R, et al. Expression of Slug is regulated by c-Myb and is required for invasion and bone marrow homing of cancer cells of different origin. J Biol Chem 2010; 285:29434-45;PMID:20622260; DOI:10.1074/jbc.M109.089045.
73. Quintana AM, Liu F, O'Rourke JP, Ness SA. Identification and regulation of c-Myb target genes in MCF-7 cells. BMC Cancer 2011; 11:30;PMID:21261996; DOI:10.1186/1471-2407-11-30.
74. Guérin M, Sheng ZM, Andrieu N, Riou G. Strong association between c-myb and oestrogen-receptor expression in human breast cancer. Oncogene 1990; 5:131-5; PMID:2181374.
75. Salomoni P, Perrotti D, Martinez R, Franceschi C, Calabretta B. Resistance to apoptosis in CTLL-2 cells constitutively expressing c-Myb is associated with induction of BCL-2 expression and Myb-dependent regulation of bcl-2 promoter activity. Proc Natl Acad Sci USA 1997; 94:3296-301;PMID:9096387; DOI:10.1073/pnas.94.7.3296.
76. Zhang M, Zhang Z, Pan HY, Wang DX, Deng ZT, Ye XL. TGFbeta1 induces human bronchial epithelial cell-to-mesenchymal transition in vitro. Lung 2009; 187:187-94;PMID:19252942; DOI:10.1007/s00408-009-9139-5.
77. Wieser R, Wrana JL, Massague J. GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGFbeta receptor complex. EMBO J 1995; 14:2199-208; PMID:7774578.
78. Thullberg M, Stromblad S. Anchorage-independent cytokinesis as part of oncogenic transformation? Cell Cycle 2008; 7:984-8;PMID:18414025; DOI:10.4161/cc.7.8.5674.
79. Jänicke RU, Sprengart ML, Wati MR, Porter AG. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 1998; 273:9357-60;PMID:9545256; DOI:10.1074/jbc.273.16.9357.
80. Asiedu MK, Ingle JN, Behrens MD, Radisky DC, Knutson KL. TGF{beta}/TNF{alpha}-Mediated Epithelial-Mesenchymal Transition Generates Breast Cancer Stem Cells with a Claudin-Low Phenotype. Cancer Res 2011; 71:4707-19;PMID:21555371; DOI:10.1158/0008-5472.CAN-10-4554.
81. Korpal M, Lee ES, Hu G, Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 2008; 283:14910-4;PMID:18411277; DOI:10.1074/jbc.C800074200.
82. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, et al. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 2007; 131:146-59;PMID:17923094; DOI:10.1016/j. cell.2007.07.021.
83. Zhao H, Kalota A, Jin S, Gewirtz AM. The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood 2009; 113:505-16;PMID:18818396; DOI:10.1182/blood- 2008-01-136218.
84. Barrallo-Gimeno A, Nieto MA. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 2005; 132:3151-61;PMID:15983400; DOI:10.1242/dev.01907.
85. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, Sciammas R, et al. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 2006; 126:755-66;PMID:16923394; DOI:10.1016/j.cell.2006.06.052.
86. Drabsch Y, Robert RG, Gonda TJ. MYB suppresses differentiation and apoptosis of human breast cancer cells. Breast Cancer Res 2010; 12:55;PMID:20659323; DOI:10.1186/bcr2614.
87. Nicolau M, Levine AJ, Carlsson G. Topology based data analysis identifies a subgroup of breast cancers with a unique mutational profile and excellent survival. Proc Natl Acad Sci USA 2011; 108:7265-70;PMID:21482760; DOI:10.1073/pnas.1102826108.
88. Yang L, Pang Y, Moses HL. TGFbeta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol 2010; 31:220-7;PMID:20538542; DOI:10.1016/j.it.2010.04.002.
89. Kanzaki S, Hilliker S, Baylink DJ, Mohan S. Evidence that human bone cells in culture produce insulin-like growth factor-binding protein-4 and -5 proteases. Endocrinology 1994; 134:383-92;PMID:7506211; DOI:10.1210/en.134.1. 383.
90. Lüscher B, Eisenman RN. c-myc and c-myb protein degradation: effect of metabolic inhibitors and heat shock. Mol Cell Biol 1988; 8:2504-12; PMID:3043180.
91. McNeill RE, Miller N, Kerin MJ. Evaluation and validation of candidate endogenous control genes for real-time quantitative PCR studies of breast cancer. BMC Mol Biol 2007; 8:107;PMID:18042273; DOI:10.1186/1471-2199-8-107.
92. Vitali R, Mancini C, Cesi V, Tanno B, Mancuso M, Bossi G, et al. Slug (SNAI2) downregulation by RNA interference facilitates apoptosis and inhibits invasive growth in neuroblastoma preclinical models. Clin Cancer Res 2008; 14:4622-30;PMID:18628477; DOI:10.1158/1078-0432.CCR-07-5210.