Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Lee, Jong Kuen ^a   Park, Sae Ra ^a   Jung, Bong Kwang ^a   Jeon, Yoon Kyung ^a   Lee, Yeong Shin ^a   Kim, Min Kyoung ^a   Kim, Yong Goo ^a   Jang, Ji Young ^a   Kim, Chul Woo ^a  

^a Seoul National University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXOSOMES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICRORNAS; NEOVASCULARIZATION, PATHOLOGIC; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84894211631     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084256     Document Type: Article

References (45)

1. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, et al. (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183: 1161-1172. (Pubitemid 26113979)
2. Viaud S, Ullrich E, Zitvogel L, Chaput N (2008) Exosomes for the treatment of human malignancies. Horm Metab Res 40: 82-88. (Pubitemid 351363418)
3. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659. (Pubitemid 47214727)
4. Camussi G, Deregibus MC, Bruno S, Grange C, Fonsato V, et al. (2011) Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am J Cancer Res 1: 98-110.
5. Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11: 228-234.
6. Garofalo M, Croce CM (2011) microRNAs: Master regulators as potential therapeutics in cancer. Annu Rev Pharmacol Toxicol 51: 25-43.
7. Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, et al. (2011) Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 71: 5346-5356.
8. Yang M, Chen J, Su F, Yu B, Lin L, et al. (2011) Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 10: 117.
9. Kosaka N, Iguchi H, Ochiya T (2010) Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 101: 2087-2092.
10. Yang C, Wang C, Chen X, Chen S, Zhang Y, et al. (2012) Identification of seven serum microRNAs from a genome-wide serum microRNA expression profile as potential noninvasive biomarkers for malignant astrocytomas. Int J Cancer.
11. Uccelli A, Moretta L, Pistoia V (2008) Mesenchymal stem cells in health and disease. Nat Rev Immunol 8: 726-736.
12. Bergfeld SA, DeClerck YA (2010) Bone marrow-derived mesenchymal stem cells and the tumor microenvironment. Cancer Metastasis Rev 29: 249-261.
13. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, et al. (2003) Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102: 3837-3844. (Pubitemid 37409409)
14. Galie M, Konstantinidou G, Peroni D, Scambi I, Marchini C, et al. (2008) Mesenchymal stem cells share molecular signature with mesenchymal tumor cells and favor early tumor growth in syngeneic mice. Oncogene 27: 2542-2551. (Pubitemid 351550885)
15. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, et al. (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449: 557-563. (Pubitemid 47525152)
16. Khakoo AY, Pati S, Anderson SA, Reid W, Elshal MF, et al. (2006) Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J Exp Med 203: 1235-1247. (Pubitemid 43736593)
17. Zhu Y, Sun Z, Han Q, Liao L, Wang J, et al. (2009) Human mesenchymal stem cells inhibit cancer cell proliferation by secreting DKK-1. Leukemia 23: 925-933.
18. Klopp AH, Gupta A, Spaeth E, Andreeff M, Marini F 3rd (2011) Concise review: Dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem Cells 29: 11-19.
19. Wang S, Olson EN (2009) AngiomiRs - key regulators of angiogenesis. Curr Opin Genet Dev 19: 205-211.
20. Borgstrom P, Hillan KJ, Sriramarao P, Ferrara N (1996) Complete inhibition of angiogenesis and growth of microtumors by anti-vascular endothelial growth factor neutralizing antibody: novel concepts of angiostatic therapy from intravital videomicroscopy. Cancer Res 56: 4032-4039. (Pubitemid 26284756)
21. Beckermann BM, Kallifatidis G, Groth A, Frommhold D, Apel A, et al. (2008) VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br J Cancer 99: 622-631.
22. Wu Y, Chen L, Scott PG, Tredget EE (2007) Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 25: 2648-2659. (Pubitemid 47582758)
23. Ho IA, Toh HC, Ng WH, Teo YL, Guo CM, et al. (2012) Human Bone Marrow-Derived Mesenchymal Stem Cells Suppress Human Glioma Growth Through Inhibition of Angiogenesis. Stem Cells.
24. Otsu K, Das S, Houser SD, Quadri SK, Bhattacharya S, et al. (2009) Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells. Blood 113: 4197-4205.
25. Cho JA, Lee YS, Kim SH, Ko JK, Kim CW (2009) MHC independent antitumor immune responses induced by Hsp70-enriched exosomes generate tumor regression in murine models. Cancer Lett 275: 256-265.
26. Kogure T, Lin WL, Yan IK, Braconi C, Patel T (2011) Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 54: 1237-1248.
27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
28. Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, et al. (2010) Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One 5: e11803.
29. Itoh T, Tanioka M, Yoshida H, Yoshioka T, Nishimoto H, et al. (1998) Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res 58: 1048-1051. (Pubitemid 28182477)
30. Wagatsuma A (2007) Endogenous expression of angiogenesis-related factors in response to muscle injury. Mol Cell Biochem 298: 151-159.
31. Lee YS, Kim SH, Cho JA, Kim CW (2011) Introduction of the CIITA gene into tumor cells produces exosomes with enhanced anti-tumor effects. Exp Mol Med 43: 281-290.
32. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, et al. (2009) Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 4: e4722.
33. McMahon G (2000) VEGF receptor signaling in tumor angiogenesis. Oncologist 5 Suppl 1: 3-10.
34. Wu Y, Hooper AT, Zhong Z, Witte L, Bohlen P, et al. (2006) The vascular endothelial growth factor receptor (VEGFR-1) supports growth and survival of human breast carcinoma. Int J Cancer 119: 1519-1529. (Pubitemid 44258756)
35. Zhu W, Huang L, Li Y, Zhang X, Gu J, et al. (2012) Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo. Cancer Lett 315: 28-37.
36. Roland CL, Lynn KD, Toombs JE, Dineen SP, Udugamasooriya DG, et al. (2009) Cytokine levels correlate with immune cell infiltration after anti-VEGF therapy in preclinical mouse models of breast cancer. PLoS One 4: e7669.
37. Chamorro-Jorganes A, Araldi E, Penalva LO, Sandhu D, Fernandez-Hernando C, et al. (2011) MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler Thromb Vasc Biol 31: 2595-2606.
38. Dejean E, Renalier MH, Foisseau M, Agirre X, Joseph N, et al. (2011) Hypoxia-microRNA-16 downregulation induces VEGF expression in anaplastic lymphoma kinase (ALK)-positive anaplastic large-cell lymphomas. Leukemia 25: 1882-1890.
39. Hua Z, Lv Q, Ye W, Wong CK, Cai G, et al. (2006) MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One 1: e116.
40. Dvorak HF, Nagy JA, Feng D, Brown LF, Dvorak AM (1999) Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr Top Microbiol Immunol 237: 97-132. (Pubitemid 28554861)
41. Bernatchez PN, Soker S, Sirois MG (1999) Vascular endothelial growth factor effect on endothelial cell proliferation, migration, and platelet-activating factor synthesis is Flk-1-dependent. J Biol Chem 274: 31047-31054.
42. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L (2006) VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371.
43. Yu H, Wu J, Li H, Wang Z, Chen X, et al. (2007) Inhibition of corneal neovascularization by recombinant adenovirus-mediated sFlk-1 expression. Biochem Biophys Res Commun 361: 946-952. (Pubitemid 47259027)
44. Camussi G, Deregibus MC, Tetta C (2012) Tumor-Derived Microvesicles and the Cancer Microenvironment. Curr Mol Med.
45. Hall B, Andreeff M, Marini F (2007) The participation of mesenchymal stem cells in tumor stroma formation and their application as targeted-gene delivery vehicles. Handb Exp Pharmacol: 263-283.