Stromal miR-200s contribute to breast cancer cell invasion through CAF activation and ECM remodeling

Cell Death and Differentiation

Volumn 23, Issue 1, 2016, Pages 132-145

  Tang, X ^a   Hou, Y ^a   Yang, G ^a   Wang, X ^a   Tang, S ^a   Du, Y E ^a   Yang, L ^a   Yu, T ^a   Zhang, H ^a   Zhou, M ^a   Wen, S ^a   Xu, L ^a   Liu, M ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; FIBRONECTIN; MICRORNA 200; PROTEIN LYSINE 6 OXIDASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR TCF12; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CELL RECEPTOR; FLII PROTEIN, HUMAN; MICRORNA; MIRN200 MICRORNA, HUMAN; TCF12 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; BREAST METASTASIS; CANCER ASSOCIATED FIBROBLAST; CANCER TISSUE; CELL DIFFERENTIATION; CELL INVASION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT; UPREGULATION; BREAST TUMOR; CELL MOTION; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METABOLISM; PATHOLOGY; SECONDARY; TUMOR INVASION; XENOGRAFT;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; FIBRONECTINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; MICROFILAMENT PROTEINS; MICRORNAS; NEOPLASM INVASIVENESS; PROTEIN-LYSINE 6-OXIDASE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TUMOR MICROENVIRONMENT;

EID: 84949534759     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2015.78     Document Type: Article

References (48)

1. Paszek MJ, Weaver VM. The tension mounts: mechanics meets morphogenesis and malignancy. J Mammary Gland Biol Neoplasia 2004; 9: 325-342.
2. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005; 8: 241-254.
3. Zaman MH, Trapani LM, Sieminski AL, Mackellar D, Gong H, Kamm RD., et al. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci USA 2006; 103: 10889-10894.
4. Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E., et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011; 146: 148-163.
5. Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI., et al. Mechanotransduction and YAP-Dependent matrix remodelling is required for the generation and maintenance of cancer-Associated fibroblasts. Nat Cell Biol 2013; 15: 637-646.
6. Zhao L, Sun Y, Hou Y, Peng Q, Wang L, Luo H., et al. MiRNA expression analysis of cancerassociated fibroblasts and normal fibroblasts in breast cancer. Int J Biochem Cell Biol 2012; 44: 2051-2059.
7. Oba S, Kumano S, Suzuki E, Nishimatsu H, Takahashi M, Takamori H., et al. miR-200b precursor can ameliorate renal tubulointerstitial fibrosis. PLoS One 2010; 5: e13614.
8. Chen Y, Ge W, Xu L, Qu C, Zhu M, Zhang W., et al. miR-200b is involved in intestinal fibrosis of Crohn's disease. Int J Mol Med 2012; 29: 601-606.
9. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S., et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMTand invasion in cancer cells. EMBO Rep 2008; 9: 582-589.
10. Saydam O, Shen Y, Wurdinger T, Senol O, Boke E, James MF., et al. Downregulated microRNA-200a in meningiomas promotes tumor growth by reducing E-cadherin and activating the Wnt/beta-catenin signaling pathway. Mol Cell Biol 2009; 29: 5923-5940.
11. 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: 14910-14914.
12. Howe EN, Cochrane DR, Richer JK. Targets of miR-200c mediate suppression of cell motility and anoikis resistance. Breast Cancer Res 2011; 13: R45.
13. Chen J, Tian W, Cai H, He H, Deng Y. Down-regulation of microRNA-200c is associated with drug resistance in human breast cancer. Med Oncol 2012; 29: 2527-2534.
14. Aydogdu E, Katchy A, Tsouko E, Lin CY, Haldosen LA, Helguero L., et al. MicroRNAregulated gene networks during mammary cell differentiation are associated with breast cancer. Carcinogenesis 2012; 33: 1502-1511.
15. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D., et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009; 138: 592-603.
16. Lin CH, Jackson AL, Guo J, Linsley PS, Eisenman RN. Myc-regulated microRNAs attenuate embryonic stem cell differentiation. EMBO J 2009; 28: 3157-3170.
17. Kojima Y, Acar A, Eaton EN, Mellody KT, Scheel C, Ben-Porath I., et al. Autocrine TGF-beta and stromal cell-Derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc Natl Acad Sci USA 2010; 107: 20009-20014.
18. Rokavec M, Wu W, Luo JL. IL6-mediated suppression of miR-200c directs constitutive activation of inflammatory signaling circuit driving transformation and tumorigenesis. Mol Cell 2012; 45: 777-789.
19. Gregory PA, Bracken CP, Smith E, Bert AG, Wright JA, Roslan S., et al. An autocrine TGFbeta/ ZEB/miR-200 signaling network regulates establishment and maintenance of epithelialmesenchymal transition. Mol Biol Cell 2011; 22: 1686-1698.
20. Peng Q, Zhao L, Hou Y, Sun Y, Wang L, Luo H., et al. Biological characteristics and genetic heterogeneity between carcinoma-Associated fibroblasts and their paired normal fibroblasts in human breast cancer. PLoS One 2013; 8: e60321.
21. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q., 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 2010; 123: 725-731.
22. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006; 6: 392-401.
23. Ambros V. The functions of animal microRNAs. Nature 2004; 431: 350-355.
24. Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 2012; 196: 395-406.
25. Aprelikova O, Yu X, Palla J, Wei BR, John S, Yi M., et al. The role of miR-31 and its target gene SATB2 in cancer-Associated fibroblasts. Cell Cycle 2010; 9: 4387-4398.
26. Musumeci M, Coppola V, Addario A, Patrizii M, Maugeri-Sacca M, Memeo L., et al. Control of tumor and microenvironment cross-Talk by miR-15a and miR-16 in prostate cancer. Oncogene 2011; 30: 4231-4242.
27. Mitra AK, Zillhardt M, Hua Y, Tiwari P, Murmann AE, Peter ME., et al. MicroRNAs reprogram normal fibroblasts into cancer-Associated fibroblasts in ovarian cancer. Cancer Discov 2012; 2: 1100-1108.
28. Zhang Y, Yang Z, Whitby R, Wang L. Regulation of miR-200c by nuclear receptors PPARalpha, LRH-1 and SHP. Biochem Biophys Res Commun 2011; 416: 135-139.
29. Lohr M, Schmidt C, Ringel J, Kluth M, Muller P, Nizze H., et al. Transforming growth factorbeta1 induces desmoplasia in an experimental model of human pancreatic carcinoma. Cancer Res 2001; 61: 550-555.
30. Rizvi S, Mertens JC, Bronk SF, Hirsova P, Dai H, Roberts LR., et al. Platelet-Derived growth factor primes cancer-Associated fibroblasts for apoptosis. J Biol Chem 2014; 289: 22835-22849.
31. Bao B, Wang Z, Ali S, Ahmad A, Azmi AS, Sarkar SH., et al. Metformin inhibits cell proliferation, migration and invasion by attenuating CSC function mediated by deregulating miRNAs in pancreatic cancer cells. Cancer Preven Res 2012; 5: 355-364.
32. Venneti S, Boateng LA, Friedman JR, Baldwin DA, Tobias JW, Judkins AR., et al. MiRNA-9 and MiRNA-200a distinguish hemangioblastomas from metastatic clear cell renal cell carcinomas in the CNS. Brain Pathol 2011; 22: 522-529.
33. Brown LA, Rodaway AR, Schilling TF, Jowett T, Ingham PW. Patient RK,., et al. Insights into early vasculogenesis revealed by expression of the ETS-Domain transcription factor Fli-1 in wild-Type and mutant zebrafish embryos. Mech Dev 2000; 90: 237-252.
34. Huang H, Yu M, Akie TE, Moran TB, Woo AJ, Tu N., et al. Differentiation-Dependent interactions between RUNX-1 and FLI-1 during megakaryocyte development. Mol Cell Biol 2009; 29: 4103-4115.
35. Braunstein M, Anderson MK. HEB in the spotlight: transcriptional regulation of T-cell specification, commitment, and developmental plasticity. Clin Dev Immunol 2012; 2012: 678705.
36. Liu YN, Yin JJ, Abou-Kheir W, Hynes PG, Casey OM, Fang L., et al. MiR-1 and miR-200 inhibit EMT via Slug-Dependent and tumorigenesis via Slug-independent mechanisms. Oncogene 2012; 32: 296-306.
37. Kumar MS, Hendrix JA, Johnson AD, Owens GK. Smooth muscle alpha-Actin gene requires two E-boxes for proper expression in vivo and is a target of class I basic helix-loop-helix proteins. Circ Res 2003; 92: 840-847.
38. Sussman CR, Davies JE, Miller RH. Extracellular and intracellular regulation of oligodendrocyte development: roles of Sonic hedgehog and expression of E proteins. Glia 2002; 40: 55-64.
39. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009; 139: 891-906.
40. Cukierman E, Bassi DE. Physico-mechanical aspects of extracellular matrix influences on tumorigenic behaviors. Semin Cancer Biol 2010; 20: 139-145.
41. Pfeiffer BJ, Franklin CL, Hsieh FH, Bank RA, Phillips CL. Alpha 2(I) collagen deficient oim mice have altered biomechanical integrity, collagen content, and collagen crosslinking of their thoracic aorta. Matrix Biol 2005; 24: 451-458.
42. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A., et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009; 15: 35-44.
43. Albinger-Hegyi A, Stoeckli SJ, Schmid S, Storz M, Iotzova G, Probst-Hensch NM., et al. Lysyl oxidase expression is an independent marker of prognosis and a predictor of lymph node metastasis in oral and oropharyngeal squamous cell carcinoma (OSCC). Int J Cancer 2010; 126: 2653-2662.
44. Sottile J, Hocking DC. Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol Biol Cell 2002; 13: 3546-3559.
45. Wang L, Hou Y, Sun Y, Zhao L, Tang X, Hu P., et al. c-Ski activates cancer-Associated fibroblasts to regulate breast cancer cell invasion. Mol Oncol 2013; 7: 1116-1128.
46. Hu P, Yang J, Hou Y, Zhang H, Zeng Z, Zhao L., et al. LncRNA expression signatures of twist-induced epithelial-To-mesenchymal transition in MCF10A cells. Cell Signal 2014; 26: 83-93.
47. Bonapace L, Coissieux MM,Wyckoff J, Mertz KD, Varga Z, Junt T., et al. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature 2014; 515: 130-133.
48. Shree T, Olson OC, Elie BT, Kester JC, Garfall AL, Simpson K., et al. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev 2011; 25: 2465-2479.