Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier

Nature Communications

Volumn 6, Issue , 2015, Pages

  Tominaga, Naoomi ^a,b,c   Kosaka, Nobuyoshi ^a,c,d   Ono, Makiko ^a   Katsuda, Takeshi ^a   Yoshioka, Yusuke ^a   Tamura, Kenji ^a   Lötvall, Jan ^e   Nakagama, Hitoshi ^a,b   Ochiya, Takahiro ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COFILIN; MICRORNA; MICRORNA 181C; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; UNCLASSIFIED DRUG; 3 PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE; ACTIN DEPOLYMERIZING FACTOR; MIRN181 MICRORNA, HUMAN; PDPK1 PROTEIN, HUMAN;

BRAIN; CANCER; GENE EXPRESSION; GERM CELL; MOLECULAR ANALYSIS; PROTEIN; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CANCER; BRAIN METASTASIS; BREAST CANCER CELL LINE; CANCER CELL; CELL COMMUNICATION; CONTROLLED STUDY; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MEMBRANE VESICLE; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PDPK1 GENE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; ANIMAL; BRAIN TUMOR; BREAST TUMOR; CANCER TRANSPLANTATION; DOWN REGULATION; EXOSOME; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SCID MOUSE; SECONDARY; SECRETION (PROCESS); TUMOR CELL LINE;

3-PHOSPHOINOSITIDE-DEPENDENT PROTEIN KINASES; ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; DOWN-REGULATION; EXTRACELLULAR VESICLES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, SCID; MICRORNAS; NEOPLASM TRANSPLANTATION; PHOSPHORYLATION; PROTEIN TRANSPORT;

EID: 84926298898     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7716     Document Type: Article

References (31)

1. Arshad, F., Wang, L., Sy, C., Avraham, S. & Avraham, H. K. Blood-brain barrier integrity and breast cancer metastasis to the brain. Patholog. Res. Int. 2011, 920509 (2010).
2. Bos, P. D., Nguyen, D. X. & Massagué, J. Modeling metastasis in the mouse. Curr. Opin. Pharmacol. 10, 571-577 (2010).
3. Winkler, E. A., Bell, R. D. & Zlokovic, B. V. Central nervous system pericytes in health and disease. Nat. Neurosci. 14, 1398-1405 (2011).
4. Ballabh, P., Braun, A. & Nedergaard, M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 16, 1-13 (2004).
5. Lee, T. H., Avraham, H. K., Jiang, S. & Avraham, S. Vascular endothelial growth factor modulates the transendothelial migration of MDA-MB-231 breast cancer cells through regulation of brain microvascular endothelial cell permeability. J. Biol. Chem. 278, 5277-5284 (2003).
6. Nicolson, G. L. Organ specificity of tumor metastasis: role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites. Cancer. Metastasis Rev. 7, 143-188 (1988).
7. Orr, F. W., Wang, H. H., Lafrenie, R. M., Scherbarth, S. & Nance, D. M. Interactions between cancer cells and the endothelium in metastasis. J. Pathol. 190, 310-329 (2000).
8. Yano, S. et al. Expression of vascular endothelial growth factor is necessary but not sufficient for production and growth of brain metastasis. Cancer Res. 60, 4959-4967 (2000).
9. Yang, C. & Robbins, P. D. The roles of tumor-derived exosomes in cancer pathogenesis. Clin. Dev. Immunol. 2011, 842849 (2011).
10. Bobrie, A. et al. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res. 72, 4920-4930 (2012).
11. Peinado, H. et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18, 883-891 (2012).
12. Valadi, H. et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659 (2007).
13. Bos, P. D. et al. Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005-1009 (2009).
14. Kosaka, N. et al. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J. Biol. Chem. 288, 10849-10859 (2013).
15. Zhou, W. et al. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell 25, 501-515 (2014).
16. Gaillard, P. J. et al. Establishment and functional characterization of an in vitro model of the blood-brain barrier, comprising a co-culture of brain capillary endothelial cells and astrocytes. Eur. J. Pharm. Sci. 12, 215-222 (2001).
17. Wilhelm, I., Fazakas, C. & Krizbai, I. A. In vitro models of the blood-brain barrier. Acta Neurobiol. Exp. (Wars) 71, 113-128 (2011).
18. Caby, M. P., Lankar, D., Vincendeau-Scherrer, C., Raposo, G. & Bonnerot, C. Exosomal-like vesicles are present in human blood plasma. Int. Immunol. 17, 879-887 (2005).
19. Nakagawa, S. et al. A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes. Neurochem. Int. 54, 253-263 (2009).
20. Ostrowski, M. et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12, 19-30 sup pp 11-13 (2010).
21. Lyle, A. N. & Griendling, K. K. Modulation of vascular smooth muscle signaling by reactive oxygen species. Physiology (Bethesda) 21, 269-280 (2006).
22. Higuchi, M., Onishi, K., Kikuchi, C. & Gotoh, Y. Scaffolding function of PAK in the PDK1-Akt pathway. Nat. Cell Biol. 10, 1356-1364 (2008).
23. Zaru, R., Mollahan, P. & Watts, C. 3-phosphoinositide-dependent kinase 1 deficiency perturbs Toll-like receptor signaling events and actin cytoskeleton dynamics in dendritic cells. J. Biol. Chem. 283, 929-939 (2008).
24. Lu, Z., Cox-Hipkin, M. A., Windsor, W. T. & Boyapati, A. 3-phosphoinositide-dependent protein kinase-1 regulates proliferation and survival of cancer cells with an activated mitogen-activated protein kinase pathway. Mol. Cancer Res. 8, 421-432 (2010).
25. Ji, J. et al. Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology 50, 472-480 (2009).
26. Sand, M. et al. Expression of microRNAs in basal cell carcinoma. Br. J. Dermatol. 167, 847-855 (2012).
27. Lowery, A. J. et al. MicroRNA signatures predict oestrogen receptor, progesterone receptor and HER2/neu receptor status in breast cancer. Breast Cancer Res. 11, R27 (2009).
28. Brown, H. et al. Evidence of blood-brain barrier dysfunction in human cerebral malaria. Neuropathol. Appl. Neurobiol. 25, 331-340 (1999).
29. Abbott, N. J., Rönnbäck, L. & Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53 (2006).
30. Polimeni, M. & Prato, M. Host matrix metalloproteinases in cerebral malaria: new kids on the block against blood-brain barrier integrity? Fluids Barriers CNS 11, 1 (2014).
31. Kis, B. et al. Adrenomedullin regulates blood-brain barrier functions in vitro. Neuroreport 12, 4139-4142 (2001).