Cancer-Secreted miR-105 destroys vascular endothelial barriers to promote metastasis

Cancer Cell

Volumn 25, Issue 4, 2014, Pages 501-515

  Zhou, Weiying ^a,b   Fong, Miranda Y ^a   Min, Yongfen ^e   Somlo, George ^a   Liu, Liang ^a,c   Palomares, Melanie R ^a   Yu, Yang ^a,c   Chow, Amy ^a   O'Connor, Sean Timothy Francis ^a   Chin, Andrew R ^a   Yen, Yun ^a   Wang, Yafan ^a   Marcusson, Eric G ^d   Chu, Peiguo ^a   Wu, Jun ^a   Wu, Xiwei ^a   Li, Arthur Xuejun ^a   Li, Zhuo ^a   Gao, Hanlin ^a   Ren, Xiubao ^c   Boldin, Mark P ^a   Lin, Pengnian Charles ^e   Wang, Shizhen Emily ^a   more..

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d REGULUS THERAPEUTICS   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 105; PROTEIN ZO1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL PERMEABILITY; BREAST METASTASIS; CANCER CELL; CANCER GROWTH; CANCER PATIENT; CANCER STAGING; CONTROLLED STUDY; EARLY CANCER; EXOSOME; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; TIGHT JUNCTION; VASCULAR ENDOTHELIUM;

BREAST NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL MOVEMENT; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; MICRORNAS; NEOPLASM METASTASIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84898476721     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2014.03.007     Document Type: Article

References (60)

1. Arroyo J.D., Chevillet J.R., Kroh E.M., Ruf I.K., Pritchard C.C., Gibson D.F., Mitchell P.S., Bennett C.F., Pogosova-Agadjanyan E.L., Stirewalt D.L., et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. USA 2011, 108:5003-5008.
2. Benakanakere M.R., Li Q., Eskan M.A., Singh A.V., Zhao J., Galicia J.C., Stathopoulou P., Knudsen T.B., Kinane D.F. Modulation of TLR2 protein expression by miR-105 in human oral keratinocytes. J.Biol. Chem. 2009, 284:23107-23115.
3. Brennan K., Offiah G., McSherry E.A., Hopkins A.M. Tight junctions: a barrier to the initiation and progression of breast cancer?. J.Biomed. Biotechnol. 2010, 2010:460607.
4. Calin G.A., Croce C.M. MicroRNA signatures in human cancers. Nat. Rev. Cancer 2006, 6:857-866.
5. Chambers A.F., Groom A.C., MacDonald I.C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2002, 2:563-572.
6. Citi S., Spadaro D., Schneider Y., Stutz J., Pulimeno P. Regulation of small GTPases at epithelial cell-cell junctions. Mol. Membr. Biol. 2011, 28:427-444.
7. Connolly J.O., Simpson N., Hewlett L., Hall A. Rac regulates endothelial morphogenesis and capillary assembly. Mol. Biol. Cell 2002, 13:2474-2485.
8. Davis S., Lollo B., Freier S., Esau C. Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res. 2006, 34:2294-2304.
9. Elhassan M.O., Christie J., Duxbury M.S. Homo sapiens systemic RNA interference-defective-1 transmembrane family member 1 (SIDT1) protein mediates contact-dependent small RNA transfer and microRNA-21-driven chemoresistance. J.Biol. Chem. 2012, 287:5267-5277.
10. Fabbri M., Paone A., Calore F., Galli R., Gaudio E., Santhanam R., Lovat F., Fadda P., Mao C., Nuovo G.J., et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. USA 2012, 109:E2110-E2116.
11. Georgiadis A., Tschernutter M., Bainbridge J.W., Balaggan K.S., Mowat F., West E.L., Munro P.M., Thrasher A.J., Matter K., Balda M.S., Ali R.R. The tight junction associated signalling proteins ZO-1 and ZONAB regulate retinal pigment epithelium homeostasis in mice. PLoS ONE 2010, 5:e15730.
12. González-Mariscal L., Tapia R., Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim. Biophys. Acta 2008, 1778:729-756.
13. Heneghan H.M., Miller N., Lowery A.J., Sweeney K.J., Newell J., Kerin M.J. Circulating microRNAs as novel minimally invasive biomarkers for breast cancer. Ann. Surg. 2010, 251:499-505.
14. Honeywell D.R., Cabrita M.A., Zhao H., Dimitroulakos J., Addison C.L. miR-105 inhibits prostate tumour growth by suppressing CDK6 levels. PLoS ONE 2013, 8:e70515.
15. Hood J.L., San R.S., Wickline S.A. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 2011, 71:3792-3801.
16. Hu M., Yao J., Carroll D.K., Weremowicz S., Chen H., Carrasco D., Richardson A., Violette S., Nikolskaya T., Nikolsky Y., et al. Regulation of insitu to invasive breast carcinoma transition. Cancer Cell 2008, 13:394-406.
17. Huang Y., Song N., Ding Y., Yuan S., Li X., Cai H., Shi H., Luo Y. Pulmonary vascular destabilization in the premetastatic phase facilitates lung metastasis. Cancer Res. 2009, 69:7529-7537.
18. Iorio M.V., Ferracin M., Liu C.G., Veronese A., Spizzo R., Sabbioni S., Magri E., Pedriali M., Fabbri M., Campiglio M., et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005, 65:7065-7070.
19. Itoh M., Bissell M.J. The organization of tight junctions in epithelia: implications for mammary gland biology and breast tumorigenesis. J.Mammary Gland Biol. Neoplasia 2003, 8:449-462.
20. Jou T.S., Schneeberger E.E., Nelson W.J. Structural and functional regulation of tight junctions by RhoA and Rac1 small GTPases. J.Cell Biol. 1998, 142:101-115.
21. Jung E.J., Santarpia L., Kim J., Esteva F.J., Moretti E., Buzdar A.U., Di Leo A., Le X.F., Bast R.C., Park S.T., et al. Plasma microRNA 210 levels correlate with sensitivity to trastuzumab and tumor presence in breast cancer patients. Cancer 2012, 118:2603-2614.
22. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
23. Kosaka N., Iguchi H., Yoshioka Y., Hagiwara K., Takeshita F., Ochiya T. Competitive interactions of cancer cells and normal cells via secretory microRNAs. J.Biol. Chem. 2012, 287:1397-1405.
24. Lee E.J., Baek M., Gusev Y., Brackett D.J., Nuovo G.J., Schmittgen T.D. Systematic evaluation of microRNA processing patterns in tissues, cell lines, and tumors. RNA 2008, 14:35-42.
25. Luga V., Zhang L., Viloria-Petit A.M., Ogunjimi A.A., Inanlou M.R., Chiu E., Buchanan M., Hosein A.N., Basik M., Wrana J.L. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 2012, 151:1542-1556.
26. Martin T.A., Jiang W.G. Loss of tight junction barrier function and its role in cancer metastasis. Biochim. Biophys. Acta 2009, 1788:872-891.
27. Martin T.A., Watkins G., Mansel R.E., Jiang W.G. Loss of tight junction plaque molecules in breast cancer tissues is associated with a poor prognosis in patients with breast cancer. Eur. J. Cancer 2004, 40:2717-2725.
28. Miller F.R., Santner S.J., Tait L., Dawson P.J. MCF10DCIS.com xenograft model of human comedo ductal carcinoma insitu. J.Natl. Cancer Inst. 2000, 92:1185-1186.
29. Mitchell P.S., Parkin R.K., Kroh E.M., Fritz B.R., Wyman S.K., Pogosova-Agadjanyan E.L., Peterson A., Noteboom J., O'Briant K.C., Allen A., et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. USA 2008, 105:10513-10518.
30. Newman A.C., Nakatsu M.N., Chou W., Gershon P.D., Hughes C.C. The requirement for fibroblasts in angiogenesis: fibroblast-derived matrix proteins are essential for endothelial cell lumen formation. Mol. Biol. Cell 2011, 22:3791-3800.
31. Nicolini A., Giardino R., Carpi A., Ferrari P., Anselmi L., Colosimo S., Conte M., Fini M., Giavaresi G., Berti P., Miccoli P. Metastatic breast cancer: an updating. Biomed. Pharmacother. 2006, 60:548-556.
32. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1889, 133:571-573.
33. Peinado H., Alečković M., Lavotshkin S., Matei I., Costa-Silva B., Moreno-Bueno G., Hergueta-Redondo M., Williams C., García-Santos G., Ghajar C., et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 2012, 18:883-891.
34. Pigati L., Yaddanapudi S.C., Iyengar R., Kim D.J., Hearn S.A., Danforth D., Hastings M.L., Duelli D.M. Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS ONE 2010, 5:e13515.
35. Podsypanina K., Du Y.C., Jechlinger M., Beverly L.J., Hambardzumyan D., Varmus H. Seeding and propagation of untransformed mouse mammary cells in the lung. Science 2008, 321:1841-1844.
36. Polette M., Gilles C., Nawrocki-Raby B., Lohi J., Hunziker W., Foidart J.M., Birembaut P. Membrane-type 1 matrix metalloproteinase expression is regulated by zonula occludens-1 in human breast cancer cells. Cancer Res. 2005, 65:7691-7698.
37. Psaila B., Lyden D. The metastatic niche: adapting the foreign soil. Nat. Rev. Cancer 2009, 9:285-293.
38. Redis R.S., Calin S., Yang Y., You M.J., Calin G.A. Cell-to-cell miRNA transfer: from body homeostasis to therapy. Pharmacol. Ther. 2012, 136:169-174.
39. Roth C., Rack B., Müller V., Janni W., Pantel K., Schwarzenbach H. Circulating microRNAs as blood-based markers for patients with primary and metastatic breast cancer. Breast Cancer Res. 2010, 12:R90.
40. Rubens R.D. 7. Management of advanced breast cancer. Int. J. Clin. Pract. 2001, 55:676-679.
41. Sethi N., Kang Y. Unravelling the complexity of metastasis - molecular understanding and targeted therapies. Nat. Rev. Cancer 2011, 11:735-748.
42. Shen L., Black E.D., Witkowski E.D., Lencer W.I., Guerriero V., Schneeberger E.E., Turner J.R. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J.Cell Sci. 2006, 119:2095-2106.
43. Skog J., Würdinger T., van Rijn S., Meijer D.H., Gainche L., Sena-Esteves M., Curry W.T., Carter B.S., Krichevsky A.M., Breakefield X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10:1470-1476.
44. Taylor D.D., Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 2008, 110:13-21.
45. Théry C., Zitvogel L., Amigorena S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2002, 2:569-579.
46. Thery C., Amigorena S., Raposo G., Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 2006, Chapter 3, Unit 3.22.
47. Tsuyada A., Chow A., Wu J., Somlo G., Chu P., Loera S., Luu T., Li A.X., Wu X., Ye W., et al. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res. 2012, 72:2768-2779.
48. Turchinovich A., Weiz L., Langheinz A., Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011, 39:7223-7233.
49. Valadi H., Ekström K., Bossios A., Sjöstrand M., Lee J.J., Lötvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
50. Vickers K.C., Remaley A.T. Lipid-based carriers of microRNAs and intercellular communication. Curr. Opin. Lipidol. 2012, 23:91-97.
51. Vickers K.C., Palmisano B.T., Shoucri B.M., Shamburek R.D., Remaley A.T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 2011, 13:423-433.
52. Wang S.E., Narasanna A., Perez-Torres M., Xiang B., Wu F.Y., Yang S., Carpenter G., Gazdar A.F., Muthuswamy S.K., Arteaga C.L. HER2 kinase domain mutation results in constitutive phosphorylation and activation of HER2 and EGFR and resistance to EGFR tyrosine kinase inhibitors. Cancer Cell 2006, 10:25-38.
53. Wang Y., Yu Y., Tsuyada A., Ren X., Wu X., Stubblefield K., Rankin-Gee E.K., Wang S.E. Transforming growth factor-β regulates the sphere-initiating stem cell-like feature in breast cancer through miRNA-181 and ATM. Oncogene 2011, 30:1470-1480.
54. Wu X., Somlo G., Yu Y., Palomares M.R., Li A.X., Zhou W., Chow A., Yen Y., Rossi J.J., Gao H., et al. De novo sequencing of circulating miRNAs identifies novel markers predicting clinical outcome of locally advanced breast cancer. J.Transl. Med. 2012, 10:42.
55. Yardley D.A. Visceral disease in patients with metastatic breast cancer: efficacy and safety of treatment with ixabepilone and other chemotherapeutic agents. Clin. Breast Cancer 2010, 10:64-73.
56. Yu Y., Wang Y., Ren X., Tsuyada A., Li A., Liu L.J., Wang S.E. Context-dependent bidirectional regulation of the MutS homolog 2 by transforming growth factor β contributes to chemoresistance in breast cancer cells. Mol. Cancer Res. 2010, 8:1633-1642.
57. Yuan A., Farber E.L., Rapoport A.L., Tejada D., Deniskin R., Akhmedov N.B., Farber D.B. Transfer of microRNAs by embryonic stem cell microvesicles. PLoS ONE 2009, 4:e4722.
58. Zhang Y., Liu D., Chen X., Li J., Li L., Bian Z., Sun F., Lu J., Yin Y., Cai X., et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol. Cell 2010, 39:133-144.
59. Zhu W., Qin W., Atasoy U., Sauter E.R. Circulating microRNAs in breast cancer and healthy subjects. BMC Res. Notes 2009, 2:89.
60. Zhuang G., Wu X., Jiang Z., Kasman I., Yao J., Guan Y., Oeh J., Modrusan Z., Bais C., Sampath D., Ferrara N. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J. 2012, 31:3513-3523.