Exosomal shuttling of miR-126 in endothelial cells modulates adhesive and migratory abilities of chronic myelogenous leukemia cells

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Taverna, Simona ^a   Amodeo, Valeria ^a   Saieva, Laura ^a   Russo, Antonio ^a   Giallombardo, Marco ^a   De Leo, Giacomo ^a   Alessandro, Riccardo ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

Chronic Myelogenous Leukemia Cells; Endothelial cells; Exosomes; miRNA

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; MICRORNA 126; VASCULAR CELL ADHESION MOLECULE 1; CXCL12 PROTEIN, HUMAN; MICRORNA; MIRN126 MICRORNA, HUMAN; STROMAL CELL DERIVED FACTOR 1;

ARTICLE; CELL ADHESION; CELL FUNCTION; CELL MOTILITY; CHRONIC MYELOID LEUKEMIA; COCULTURE; COMPARATIVE STUDY; COMPUTER MODEL; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; EXOSOMAL SHUTTLING; EXOSOME; GENE CONTROL; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; MYELOID LEUKEMIA CELL LINE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA TRANSPORT; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TUMOR MICROENVIRONMENT; BIOSYNTHESIS; CELL MOTION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL;

CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL12; ENDOTHELIAL CELLS; EXOSOMES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICRORNAS; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84904072174     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-169     Document Type: Article

References (33)

1. Rowley J. A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973, 243:290-293.
2. Ahmed W, Van Etten RA. Alternative approaches to eradicating the malignant clone in chronic myeloid leukemia: tyrosine-kinase inhibitor combinations and beyond. Hematology Am Soc Hematol Educ Program 2013, 2013:189-200.
3. Cilloni D, Saglio G. Molecular pathways: BCR-ABL. Clin Cancer Res 2012, 18:930-937.
4. Corrado C, Raimondo S, Chiesi A, Ciccia F, De Leo G, Alessandro R. Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications. Int J Mol Sci 2013, 14:5338-5366.
5. Corrado C, Flugy AM, Taverna S, Raimondo S, Guggino G, Karmali R, De Leo G, Alessandro R. Carboxyamidotriazole-orotate inhibits the growth of imatinib-resistant chronic myeloid leukaemia cells and modulates exosomes-stimulated angiogenesis. PLoS One 2012, 7:e42310.
6. Mineo M, Garfield SH, Taverna S, Flugy A, De Leo G, Alessandro R, Kohn EC. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a src-dependent fashion. Angiogenesis 2011, 15:33-45.
7. Taverna S, Flugy A, Saieva L, Kohn EC, Santoro A, Meraviglia S, De Leo G, Alessandro R. Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis. Int J Cancer 2011, 130:2033-2043.
8. Kole R, Krainer AR, Altman S. RNA therapeutics: beyond RNA interference and antisense oligonucleotides. Nat Rev Drug Discov 2012, 11:125-140.
9. Umezu T, Ohyashiki K, Kuroda M, Ohyashiki JH. Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene 2013, 32:2747-2755.
10. Tadokoro H, Umezu T, Ohyashiki K, Hirano T, Ohyashiki JH. Exosomes derived from hypoxic leukemia cells enhance tube formation in endothelial cells. J Biol Chem 2013, 288:34343-34351.
11. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 2008, 15:261-271.
12. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, Ivey KN, Bruneau BG, Stainier DY. Srivastava D: miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 2008, 15:272-284.
13. Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci U S A 2008, 105:1516-1521.
14. Sharma M, Afrin F, Satija N, Tripathi RP, Gangenahalli GU. Stromal-derived factor-1/CXCR4 signaling: indispensable role in homing and engraftment of hematopoietic stem cells in bone marrow. Stem Cells Dev 2011, 20:933-946.
15. Geay JF, Buet D, Zhang Y, Foudi A, Jarrier P, Berthebaud M, Turhan AG, Vainchenker W, Louache F. p210BCR-ABL inhibits SDF-1 chemotactic response via alteration of CXCR4 signaling and down-regulation of CXCR4 expression. Cancer Res 2005, 65:2676-2683.
16. Jin L, Tabe Y, Konoplev S, Xu Y, Leysath CE, Lu H, Kimura S, Ohsaka A, Rios MB, Calvert L, Kantarjian H, Andreeff M, Konopleva M. CXCR4 up-regulation by imatinib induces chronic myelogenous leukemia (CML) cell migration to bone marrow stroma and promotes survival of quiescent CML cells. Mol Cancer Ther 2008, 7:48-58.
17. Mazo IB, Gutierrez-Ramos JC, Frenette PS, Hynes RO, Wagner DD, von Andrian UH. Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med 1998, 188:465-474.
18. Sanz-Rodriguez F, Hidalgo A, Teixido J. Chemokine stromal cell-derived factor-1alpha modulates VLA-4 integrin-mediated multiple myeloma cell adhesion to CS-1/fibronectin and VCAM-1. Blood 2001, 97:346-351.
19. Escrevente C, Keller S, Altevogt P, Costa J. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 2011, 11:108.
20. Feng D, Zhao WL, Ye YY, Bai XC, Liu RQ, Chang LF, Zhou Q, Sui SF. Cellular internalization of exosomes occurs through phagocytosis. Traffic 2010, 11:675-687.
21. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology 2007, 9:654-659.
22. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B, Simons M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008, 319:1244-1247.
23. Zhang B, Ho YW, Huang Q, Maeda T, Lin A, Lee SU, Hair A, Holyoake TL, Huettner C, Bhatia R. Altered microenvironmental regulation of leukemic and normal stem cells in chronic myelogenous leukemia. Cancer Cell 2012, 21:577-592.
24. Castells M, Thibault B, Delord JP, Couderc B. Implication of tumor microenvironment in chemoresistance: tumor-associated stromal cells protect tumor cells from cell death. Int J Mol Sci 2012, 13:9545-9571.
25. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011, 2:282.
26. Ebrahimi F, Gopalan V, Smith RA, Lam AK. miR-126 in human cancers: Clinical roles and current perspectives. Exp Mol Pathol 2014, 96:98-107.
27. Shen WF, Hu YL, Uttarwar L, Passegue E, Largman C. MicroRNA-126 regulates HOXA9 by binding to the homeobox. Mol Cell Biol 2008, 28:4609-4619.
28. Cammarata G, Augugliaro L, Salemi D, Agueli C, La Rosa M, Dagnino L, Civiletto G, Messana F, Marfia A, Bica MG, Cascio L, Floridia PM, Mineo AM, Russo M, Fabbiano F, Santoro A. Differential expression of specific microRNA and their targets in acute myeloid leukemia. Am J Hematol 2010, 85:331-339.
29. Sipkins DA, Wei X, Wu JW, Runnels JM, Cote D, Means TK, Luster AD, Scadden DT, Lin CP. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 2005, 435:969-973.
30. Salvucci O, Jiang K, Gasperini P, Maric D, Zhu J, Sakakibara S, Espigol-Frigole G, Wang S, Tosato G. MicroRNA126 contributes to granulocyte colony-stimulating factor-induced hematopoietic progenitor cell mobilization by reducing the expression of vascular cell adhesion molecule 1. Haematologica 2012, 97:818-826.
31. Burger JA, Burger M, Kipps TJ. Chronic lymphocytic leukemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells. Blood 1999, 94:3658-3667.
32. Zepeda-Moreno A, Saffrich R, Walenda T, Hoang VT, Wuchter P, Sanchez-Enriquez S, Corona-Rivera A, Wagner W, Ho AD. Modeling SDF-1-induced mobilization in leukemia cell lines. Exp Hematol 2012, 40:666-674.
33. Alessandro R, Fontana S, Giordano M, Corrado C, Colomba P, Flugy A, Santoro A, Kohn E, De Leo G. Effects of carboxyamidotriazole on in vitro models of imatinib-resistant chronic myeloid leukemia. J Cell Physiol 2008, 215:111-121.