Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization (original) (raw)

• Thiery, J.P., Acloque, H., Huang, R.Y. & Nieto, M.A. Epithelial-mesenchymal transitions in development and disease. Cell 139, 871–890 (2009).
  Article CAS PubMed Google Scholar
• Thompson, E.W. & Williams, E.D. EMT and MET in carcinoma—clinical observations, regulatory pathways and new models. Clin. Exp. Metastasis 25, 591–592 (2008).
  Article PubMed Google Scholar
• Yang, J. & Weinberg, R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818–829 (2008).
  Article CAS PubMed Google Scholar
• Chaffer, C.L., Thompson, E.W. & Williams, E.D. Mesenchymal to epithelial transition in development and disease. Cells Tissues Organs 185, 7–19 (2007).
  Article PubMed Google Scholar
• Jeschke, U. et al. Expression of E-cadherin in human ductal breast cancer carcinoma in situ, invasive carcinomas, their lymph node metastases, their distant metastases, carcinomas with recurrence and in recurrence. Anticancer Res. 27, 1969–1974 (2007).
  CAS PubMed Google Scholar
• Park, D., Karesen, R., Axcrona, U., Noren, T. & Sauer, T. Expression pattern of adhesion molecules (E-cadherin, α-, β-, γ-catenin and claudin-7), their influence on survival in primary breast carcinoma, and their corresponding axillary lymph node metastasis. APMIS 115, 52–65 (2007).
  Article CAS PubMed Google Scholar
• Bartel, D.P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Esquela-Kerscher, A. & Slack, F.J. Oncomirs—microRNAs with a role in cancer. Nat. Rev. Cancer 6, 259–269 (2006).
  Article CAS PubMed Google Scholar
• Johnson, R. et al. A microRNA-based gene dysregulation pathway in Huntington's disease. Neurobiol. Dis. 29, 438–445 (2008).
  Article CAS PubMed Google Scholar
• Huang, Q. et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat. Cell Biol. 10, 202–210 (2008).
  Article CAS PubMed Google Scholar
• Ma, L., Teruya-Feldstein, J. & Weinberg, R.A. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682–688 (2007).
  Article CAS PubMed Google Scholar
• Ma, L. et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol. 12, 247–256 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Asangani, I.A. et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27, 2128–2136 (2008).
  Article CAS PubMed Google Scholar
• Zhu, S., Si, M.L., Wu, H. & Mo, Y.Y. MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J. Biol. Chem. 282, 14328–14336 (2007).
  Article CAS PubMed Google Scholar
• Zhu, S. et al. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res. 18, 350–359 (2008).
  Article CAS PubMed Google Scholar
• Tavazoie, S.F. et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451, 147–152 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Valastyan, S. et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137, 1032–1046 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Karres, J.S., Hilgers, V., Carrera, I., Treisman, J. & Cohen, S.M. The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell 131, 136–145 (2007).
  Article CAS PubMed Google Scholar
• Samavarchi-Tehrani, P. et al. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 7, 64–77 (2010).
  Article CAS PubMed Google Scholar
• Wellner, U. et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 11, 1487–1495 (2009).
  Article CAS PubMed Google Scholar
• Shimono, Y. et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 138, 592–603 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Iliopoulos, D. et al. 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 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Schickel, R., Park, S.M., Murmann, A.E. & Peter, M.E. miR-200c regulates induction of apoptosis through CD95 by targeting FAP-1. Mol. Cell 38, 908–915 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Cochrane, D.R., Howe, E.N., Spoelstra, N.S. & Richer, J.K. Loss of miR-200c: a marker of aggressiveness and chemoresistance in female reproductive cancers. J. Oncol. 2010, 821717 (2010).
  Article PubMed Google Scholar
• Burk, U. et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582–589 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Gregory, P.A. et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593–601 (2008).
  Article CAS PubMed Google Scholar
• Korpal, M., Lee, E.S., 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. 283, 14910–14914 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Park, S.M., Gaur, A.B., Lengyel, E. & Peter, M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22, 894–907 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Gibbons, D.L. et al. Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev. 23, 2140–2151 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Olson, P. et al. MicroRNA dynamics in the stages of tumorigenesis correlate with hallmark capabilities of cancer. Genes Dev. 23, 2152–2165 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Dykxhoorn, D.M. et al. miR-200 enhances mouse breast cancer cell colonization to form distant metastases. PLoS ONE 4, e7181 (2009).
  Article PubMed PubMed Central Google Scholar
• Camps, C. et al. hsa-miR-210 Is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin. Cancer Res. 14, 1340–1348 (2008).
  Article CAS PubMed Google Scholar
• Hudis, C.A. et al. Proposal for standardized definitions for efficacy end points in adjuvant breast cancer trials: the STEEP system. J. Clin. Oncol. 25, 2127–2132 (2007).
  Article PubMed Google Scholar
• Nam, E.J. et al. MicroRNA expression profiles in serous ovarian carcinoma. Clin. Cancer Res. 14, 2690–2695 (2008).
  Article CAS PubMed Google Scholar
• Aslakson, C.J. & Miller, F.R. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 52, 1399–1405 (1992).
  CAS PubMed Google Scholar
• Yang, J. et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927–939 (2004).
  Article CAS PubMed Google Scholar
• Lou, Y. et al. Epithelial-mesenchymal transition (EMT) is not sufficient for spontaneous murine breast cancer metastasis. Dev. Dyn. 237, 2755–2768 (2008).
  Article CAS PubMed Google Scholar
• Santner, S.J. et al. Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells. Breast Cancer Res. Treat. 65, 101–110 (2001).
  Article CAS PubMed Google Scholar
• Chaffer, C.L. et al. Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res. 66, 11271–11278 (2006).
  Article CAS PubMed Google Scholar
• Bracken, C.P. et al. A double-negative feedback loop between ZEB1–SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res. 68, 7846–7854 (2008).
  Article CAS PubMed Google Scholar
• Guo, H., Ingolia, N.T., Weissman, J.S. & Bartel, D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835–840 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Györffy, B. et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res. Treat. 123, 725–731 (2010).
  Article PubMed Google Scholar
• Lang, M.R., Lapierre, L.A., Frotscher, M., Goldenring, J.R. & Knapik, E.W. Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation. Nat. Genet. 38, 1198–1203 (2006).
  Article CAS PubMed Google Scholar
• Saito, A. et al. Regulation of endoplasmic reticulum stress response by a BBF2H7-mediated Sec23a pathway is essential for chondrogenesis. Nat. Cell Biol. 11, 1197–1204 (2009).
  Article CAS PubMed Google Scholar
• Townley, A.K. et al. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J. Cell Sci. 121, 3025–3034 (2008).
  Article CAS PubMed Google Scholar
• Huang, W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat. Protoc. 4, 44–57 (2009).
  Article CAS Google Scholar
• Wang, Y. et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365, 671–679 (2005).
  Article CAS PubMed Google Scholar
• Minn, A.J. et al. Genes that mediate breast cancer metastasis to lung. Nature 436, 518–524 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• O'Donnell, K.A., Wentzel, E.A., Zeller, K.I., Dang, C.V. & Mendell, J.T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839–843 (2005).
  Article CAS PubMed Google Scholar
• Yu, Z. et al. A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J. Cell Biol. 182, 509–517 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Yu, Z. et al. microRNA 17/20 inhibits cellular invasion and tumor metastasis in breast cancer by heterotypic signaling. Proc. Natl. Acad. Sci. USA 107, 8231–8236 (2010).
  Article CAS PubMed PubMed Central Google Scholar