Skip to main content
Top
Published in: Journal of Hematology & Oncology 1/2015

Open Access 01-12-2015 | Review

Transfer of microRNAs by extracellular membrane microvesicles: a nascent crosstalk model in tumor pathogenesis, especially tumor cell-microenvironment interactions

Authors: Li Zhang, C Alexander Valencia, Biao Dong, Meng Chen, Pu-Jun Guan, Ling Pan

Published in: Journal of Hematology & Oncology | Issue 1/2015

Login to get access

Abstract

Anticancer treatments aiming at killing malignant cells have been applied for decades but have been unsuccessful at curing the disease. The modern concept of tumor microenvironment, especially angiogenesis, suggests that the tumor is not only composed of malignant cells, but also consists of other groups of cells that work together. Recently, genetic message transfer has been revealed between tumor cells and their microenvironment. The latest cell-derived vector, extracellular membrane microvesicles (EMVs), has been found to provide membrane protection and allowed to deliver genetic information beyond the cells. Additionally, EMV-associated microRNAs are involved in a variety of cellular pathways for tumor initiation and progression. Previous published reviews have focused on miRNA that included EMVs as a sensitive marker for tumor monitoring in clinical applications that are based on the alteration of their expression levels in conjunction with disease occurrence and progression. From the aspect of cellular crosstalk, this article will review the role of EMV-mediated microRNA transfer in tumor pathogenesis, including tumor treatment obstacles, history and features, and current research in inflammatory/immune pathologies, as well as in solid tumors and hematological malignancies. This nascent crosstalk model will provide a novel insight into complementing the classic mechanisms of intercellular communication and contribute to the potential therapeutic strategy via small RNA molecule-carrying EMVs for multimodality treatment of cancer.
Literature
1.
go back to reference John SP. Retinal and choroidal angiogenesis. Berlin: Springer; 2008. John SP. Retinal and choroidal angiogenesis. Berlin: Springer; 2008.
2.
go back to reference Lord EM, Penney DP, Sutherland RM, Cooper Jr RA. Morphological and functional characteristics of cells infiltrating and destroying tumor multicellular spheroids in vivo. Virchows Arch B Cell Pathol Incl Mol Pathol. 1979;31:103–16.CrossRefPubMed Lord EM, Penney DP, Sutherland RM, Cooper Jr RA. Morphological and functional characteristics of cells infiltrating and destroying tumor multicellular spheroids in vivo. Virchows Arch B Cell Pathol Incl Mol Pathol. 1979;31:103–16.CrossRefPubMed
3.
go back to reference Verloes R, Kanarek L. Tumour microenvironment studies open new perspectives for immunotherapy. Arch Int Physiol Biochim. 1976;84:420–2.PubMed Verloes R, Kanarek L. Tumour microenvironment studies open new perspectives for immunotherapy. Arch Int Physiol Biochim. 1976;84:420–2.PubMed
4.
go back to reference Ra W. Pathology of tumours. London: Butterworth; 1948. Ra W. Pathology of tumours. London: Butterworth; 1948.
5.
go back to reference Greenfield JP, Cobb WS, Lyden D. Resisting arrest: a switch from angiogenesis to vasculogenesis in recurrent malignant gliomas. J Clin Invest. 2010;120:663–7.CrossRefPubMedCentralPubMed Greenfield JP, Cobb WS, Lyden D. Resisting arrest: a switch from angiogenesis to vasculogenesis in recurrent malignant gliomas. J Clin Invest. 2010;120:663–7.CrossRefPubMedCentralPubMed
6.
go back to reference Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med. 2001;7:1194–201.CrossRefPubMed Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med. 2001;7:1194–201.CrossRefPubMed
7.
go back to reference Streubel B, Chott A, Huber D, Exner M, Jager U, Wagner O, et al. Lymphoma-specific genetic aberrations in microvascular endothelial cells in B-cell lymphomas. N Engl J Med. 2004;351:250–9.CrossRefPubMed Streubel B, Chott A, Huber D, Exner M, Jager U, Wagner O, et al. Lymphoma-specific genetic aberrations in microvascular endothelial cells in B-cell lymphomas. N Engl J Med. 2004;351:250–9.CrossRefPubMed
8.
go back to reference Hida K, Klagsbrun M. A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities. Cancer Res. 2005;65:2507–10.CrossRefPubMed Hida K, Klagsbrun M. A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities. Cancer Res. 2005;65:2507–10.CrossRefPubMed
9.
go back to reference Rigolin GM, Fraulini C, Ciccone M, Mauro E, Bugli AM, De Angeli C, et al. Neoplastic circulating endothelial cells in multiple myeloma with 13q14 deletion. Blood. 2006;107:2531–5.CrossRefPubMed Rigolin GM, Fraulini C, Ciccone M, Mauro E, Bugli AM, De Angeli C, et al. Neoplastic circulating endothelial cells in multiple myeloma with 13q14 deletion. Blood. 2006;107:2531–5.CrossRefPubMed
10.
go back to reference Akers JC, Gonda D, Kim R, Carter BS, Chen CC. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol. 2013;113:1–11.CrossRefPubMed Akers JC, Gonda D, Kim R, Carter BS, Chen CC. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol. 2013;113:1–11.CrossRefPubMed
11.
go back to reference Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 2010;78:838–48.CrossRefPubMed Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 2010;78:838–48.CrossRefPubMed
12.
go back to reference Ghosh AK, Secreto CR, Knox TR, Ding W, Mukhopadhyay D, Kay NE. Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: implications for disease progression. Blood. 2010;115:1755–64.CrossRefPubMedCentralPubMed Ghosh AK, Secreto CR, Knox TR, Ding W, Mukhopadhyay D, Kay NE. Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: implications for disease progression. Blood. 2010;115:1755–64.CrossRefPubMedCentralPubMed
13.
go back to reference Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2011;2:180.CrossRefPubMedCentralPubMed Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2011;2:180.CrossRefPubMedCentralPubMed
14.
go back to reference Chargaff E, West R. The biological significance of the thromboplastic protein of blood. J Bio Chem. 1946;166:189–97. Chargaff E, West R. The biological significance of the thromboplastic protein of blood. J Bio Chem. 1946;166:189–97.
15.
go back to reference Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967;13:269–88.CrossRefPubMed Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967;13:269–88.CrossRefPubMed
16.
go back to reference Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Bio Chem. 1987;262:9412–20. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Bio Chem. 1987;262:9412–20.
17.
go back to reference Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol. 2014;14:195–208.CrossRefPubMed Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol. 2014;14:195–208.CrossRefPubMed
18.
go back to reference Malkki H. Neuro-oncology: novel biomarkers for high-grade astrocytoma. Nat Rev Neurol. 2014;10:121.CrossRefPubMed Malkki H. Neuro-oncology: novel biomarkers for high-grade astrocytoma. Nat Rev Neurol. 2014;10:121.CrossRefPubMed
19.
go back to reference Lemoinne S, Thabut D, Housset C, Moreau R, Valla D, Boulanger CM, et al. The emerging roles of microvesicles in liver diseases. Nat Rev Gastroenterol Hepatol. 2014;11:350–61.CrossRefPubMed Lemoinne S, Thabut D, Housset C, Moreau R, Valla D, Boulanger CM, et al. The emerging roles of microvesicles in liver diseases. Nat Rev Gastroenterol Hepatol. 2014;11:350–61.CrossRefPubMed
20.
go back to reference Salih M, Zietse R, Hoorn EJ. Urinary extracellular vesicles and the kidney: biomarkers and beyond. Am J Physiol. 2014;306:F1251–9. Salih M, Zietse R, Hoorn EJ. Urinary extracellular vesicles and the kidney: biomarkers and beyond. Am J Physiol. 2014;306:F1251–9.
21.
go back to reference 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. 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.
22.
go back to reference Huang X, Yuan T, Tschannen M, Sun Z, Jacob H, Du M, et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics. 2013;14:319.CrossRefPubMedCentralPubMed Huang X, Yuan T, Tschannen M, Sun Z, Jacob H, Du M, et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics. 2013;14:319.CrossRefPubMedCentralPubMed
23.
go back to reference Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell. 2003;115:787–98.CrossRefPubMed Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell. 2003;115:787–98.CrossRefPubMed
24.
go back to reference Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120:15–20.CrossRefPubMed Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120:15–20.CrossRefPubMed
26.
go back to reference Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–9.CrossRefPubMed Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–9.CrossRefPubMed
27.
go back to reference Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE. 2008;3:e3694.CrossRefPubMedCentralPubMed Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE. 2008;3:e3694.CrossRefPubMedCentralPubMed
28.
go back to reference Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–6.CrossRefPubMedCentralPubMed Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–6.CrossRefPubMedCentralPubMed
29.
go back to reference Noerholm M, Balaj L, Limperg T, Salehi A, Zhu LD, Hochberg FH, et al. RNA expression patterns in serum microvesicles from patients with glioblastoma multiforme and controls. BMC Cancer. 2012;12:22.CrossRefPubMedCentralPubMed Noerholm M, Balaj L, Limperg T, Salehi A, Zhu LD, Hochberg FH, et al. RNA expression patterns in serum microvesicles from patients with glioblastoma multiforme and controls. BMC Cancer. 2012;12:22.CrossRefPubMedCentralPubMed
30.
go back to reference Fourcade O, Simon MF, Viode C, Rugani N, Leballe F, Ragab A, et al. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell. 1995;80:919–27.CrossRefPubMed Fourcade O, Simon MF, Viode C, Rugani N, Leballe F, Ragab A, et al. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell. 1995;80:919–27.CrossRefPubMed
31.
go back to reference Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319:1244–7.CrossRefPubMed Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319:1244–7.CrossRefPubMed
32.
go back to reference Chen X, Liang H, Zhang J, Zen K, Zhang CY. Horizontal transfer of microRNAs: molecular mechanisms and clinical applications. Protein Cell. 2012;3:28–37.CrossRefPubMed Chen X, Liang H, Zhang J, Zen K, Zhang CY. Horizontal transfer of microRNAs: molecular mechanisms and clinical applications. Protein Cell. 2012;3:28–37.CrossRefPubMed
33.
34.
go back to reference Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010;39:133–44.CrossRefPubMed Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010;39:133–44.CrossRefPubMed
35.
go back to reference Jaworski E, Narayanan A, Van Duyne R, Shabbeer-Meyering S, Iordanskiy S, Saifuddin M, et al. Human T-lymphotropic virus type 1-infected cells secrete exosomes that contain Tax protein. J Biol Chem. 2014;289:22284–305.CrossRefPubMed Jaworski E, Narayanan A, Van Duyne R, Shabbeer-Meyering S, Iordanskiy S, Saifuddin M, et al. Human T-lymphotropic virus type 1-infected cells secrete exosomes that contain Tax protein. J Biol Chem. 2014;289:22284–305.CrossRefPubMed
36.
go back to reference Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008;10:619–24.CrossRefPubMed Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008;10:619–24.CrossRefPubMed
37.
go back to reference Okoye IS, Coomes SM, Pelly VS, Czieso S, Papayannopoulos V, Tolmachova T, et al. MicroRNA-containing T-regulatory-cell-derived exosomes suppress pathogenic T helper 1 cells. Immunity. 2014;41:89–103.CrossRefPubMedCentralPubMed Okoye IS, Coomes SM, Pelly VS, Czieso S, Papayannopoulos V, Tolmachova T, et al. MicroRNA-containing T-regulatory-cell-derived exosomes suppress pathogenic T helper 1 cells. Immunity. 2014;41:89–103.CrossRefPubMedCentralPubMed
38.
go back to reference Yin W, Ouyang S, Li Y, Xiao B, Yang H. Immature dendritic cell-derived exosomes: a promise subcellular vaccine for autoimmunity. Inflammation. 2013;36:232–40.CrossRefPubMed Yin W, Ouyang S, Li Y, Xiao B, Yang H. Immature dendritic cell-derived exosomes: a promise subcellular vaccine for autoimmunity. Inflammation. 2013;36:232–40.CrossRefPubMed
39.
go back to reference Klohn PC, Castro-Seoane R, Collinge J. Exosome release from infected dendritic cells: a clue for a fast spread of prions in the periphery? J Infect. 2013;67:359–68.CrossRefPubMed Klohn PC, Castro-Seoane R, Collinge J. Exosome release from infected dendritic cells: a clue for a fast spread of prions in the periphery? J Infect. 2013;67:359–68.CrossRefPubMed
40.
go back to reference Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 2011;29:341–5.CrossRefPubMed Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 2011;29:341–5.CrossRefPubMed
41.
go back to reference Morelli AE, Larregina AT, Shufesky WJ, Sullivan ML, Stolz DB, Papworth GD, et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood. 2004;104:3257–66.CrossRefPubMed Morelli AE, Larregina AT, Shufesky WJ, Sullivan ML, Stolz DB, Papworth GD, et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood. 2004;104:3257–66.CrossRefPubMed
43.
go back to reference Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009;9:581–93.CrossRefPubMed Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009;9:581–93.CrossRefPubMed
44.
go back to reference Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009;19:43–51.CrossRefPubMed Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009;19:43–51.CrossRefPubMed
45.
go back to reference Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res. 2010;107:677–84.CrossRefPubMed Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res. 2010;107:677–84.CrossRefPubMed
46.
go back to reference Cantaluppi V, Gatti S, Medica D, Figliolini F, Bruno S, Deregibus MC, et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 2012;82:412–27.CrossRefPubMed Cantaluppi V, Gatti S, Medica D, Figliolini F, Bruno S, Deregibus MC, et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 2012;82:412–27.CrossRefPubMed
47.
go back to reference van Solingen C, de Boer HC, Bijkerk R, Monge M, van Oeveren-Rietdijk AM, Seghers L, et al. MicroRNA-126 modulates endothelial SDF-1 expression and mobilization of Sca-1(+)/Lin(−) progenitor cells in ischaemia. Cardiovasc Res. 2011;92:449–55.CrossRefPubMed van Solingen C, de Boer HC, Bijkerk R, Monge M, van Oeveren-Rietdijk AM, Seghers L, et al. MicroRNA-126 modulates endothelial SDF-1 expression and mobilization of Sca-1(+)/Lin(−) progenitor cells in ischaemia. Cardiovasc Res. 2011;92:449–55.CrossRefPubMed
48.
go back to reference Ranghino A, Cantaluppi V, Grange C, Vitillo L, Fop F, Biancone L, et al. Endothelial progenitor cell-derived microvesicles improve neovascularization in a murine model of hindlimb ischemia. Int J Immunopathol Pharmacol. 2012;25:75–85.PubMed Ranghino A, Cantaluppi V, Grange C, Vitillo L, Fop F, Biancone L, et al. Endothelial progenitor cell-derived microvesicles improve neovascularization in a murine model of hindlimb ischemia. Int J Immunopathol Pharmacol. 2012;25:75–85.PubMed
49.
go back to reference Lai RC, Arslan F, Lee MM, Sze NS, Choo A, Chen TS, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res. 2010;4:214–22.CrossRefPubMed Lai RC, Arslan F, Lee MM, Sze NS, Choo A, Chen TS, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res. 2010;4:214–22.CrossRefPubMed
50.
go back to reference Sun Q, Chen X, Yu J, Zen K, Zhang CY, Li L. Immune modulatory function of abundant immune-related microRNAs in microvesicles from bovine colostrum. Protein & cell. 2013;4:197–210.CrossRef Sun Q, Chen X, Yu J, Zen K, Zhang CY, Li L. Immune modulatory function of abundant immune-related microRNAs in microvesicles from bovine colostrum. Protein & cell. 2013;4:197–210.CrossRef
51.
go back to reference Wang G, Tam LS, Li EK, Kwan BC, Chow KM, Luk CC, et al. Serum and urinary cell-free MiR-146a and MiR-155 in patients with systemic lupus erythematosus. J Rheumatol. 2010;37:2516–22.CrossRefPubMed Wang G, Tam LS, Li EK, Kwan BC, Chow KM, Luk CC, et al. Serum and urinary cell-free MiR-146a and MiR-155 in patients with systemic lupus erythematosus. J Rheumatol. 2010;37:2516–22.CrossRefPubMed
52.
go back to reference Carlsen AL, Schetter AJ, Nielsen CT, Lood C, Knudsen S, Voss A, et al. Circulating microRNA expression profiles associated with systemic lupus erythematosus. Arthritis Rheum. 2013;65:1324–34.CrossRefPubMed Carlsen AL, Schetter AJ, Nielsen CT, Lood C, Knudsen S, Voss A, et al. Circulating microRNA expression profiles associated with systemic lupus erythematosus. Arthritis Rheum. 2013;65:1324–34.CrossRefPubMed
53.
go back to reference Wang H, Peng W, Ouyang X, Li W, Dai Y. Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Trans Res. 2012;160:198–206.CrossRef Wang H, Peng W, Ouyang X, Li W, Dai Y. Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Trans Res. 2012;160:198–206.CrossRef
54.
go back to reference Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 2010;12:247–56.PubMedCentralPubMed Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 2010;12:247–56.PubMedCentralPubMed
55.
go back to reference Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, et al. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J. 2012;31:3513–23.CrossRefPubMedCentralPubMed Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, et al. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J. 2012;31:3513–23.CrossRefPubMedCentralPubMed
56.
go back to reference Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res. 2008;18:350–9.CrossRefPubMed Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res. 2008;18:350–9.CrossRefPubMed
57.
go back to reference Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010;101:2087–92.CrossRefPubMed Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010;101:2087–92.CrossRefPubMed
58.
go back to reference Gallach S, Calabuig-Farinas S, Jantus-Lewintre E, Camps C. MicroRNAs: promising new antiangiogenic targets in cancer. BioMed Res Int. 2014;2014:878450.CrossRefPubMedCentralPubMed Gallach S, Calabuig-Farinas S, Jantus-Lewintre E, Camps C. MicroRNAs: promising new antiangiogenic targets in cancer. BioMed Res Int. 2014;2014:878450.CrossRefPubMedCentralPubMed
59.
go back to reference Yang M, Chen J, Su F, Yu B, Su F, Lin L, et al. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer. 2011;10:117.CrossRefPubMedCentralPubMed Yang M, Chen J, Su F, Yu B, Su F, Lin L, et al. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer. 2011;10:117.CrossRefPubMedCentralPubMed
60.
go back to reference Lima LG, Chammas R, Monteiro RQ, Moreira ME, Barcinski MA. Tumor-derived microvesicles modulate the establishment of metastatic melanoma in a phosphatidylserine-dependent manner. Cancer Lett. 2009;283:168–75.CrossRefPubMed Lima LG, Chammas R, Monteiro RQ, Moreira ME, Barcinski MA. Tumor-derived microvesicles modulate the establishment of metastatic melanoma in a phosphatidylserine-dependent manner. Cancer Lett. 2009;283:168–75.CrossRefPubMed
61.
go back to reference Wysoczynski M, Ratajczak MZ. Lung cancer secreted microvesicles: underappreciated modulators of microenvironment in expanding tumors. Int J Cancer. 2009;125:1595–603.CrossRefPubMedCentralPubMed Wysoczynski M, Ratajczak MZ. Lung cancer secreted microvesicles: underappreciated modulators of microenvironment in expanding tumors. Int J Cancer. 2009;125:1595–603.CrossRefPubMedCentralPubMed
62.
go back to reference Lehmann BD, Paine MS, Brooks AM, McCubrey JA, Renegar RH, Wang R, et al. Senescence-associated exosome release from human prostate cancer cells. Cancer Res. 2008;68:7864–71.CrossRefPubMed Lehmann BD, Paine MS, Brooks AM, McCubrey JA, Renegar RH, Wang R, et al. Senescence-associated exosome release from human prostate cancer cells. Cancer Res. 2008;68:7864–71.CrossRefPubMed
63.
go back to reference Hessvik NP, Phuyal S, Brech A, Sandvig K, Llorente A. Profiling of microRNAs in exosomes released from PC-3 prostate cancer cells. Biochim Biophys Acta. 2012;1819:1154–63.CrossRefPubMed Hessvik NP, Phuyal S, Brech A, Sandvig K, Llorente A. Profiling of microRNAs in exosomes released from PC-3 prostate cancer cells. Biochim Biophys Acta. 2012;1819:1154–63.CrossRefPubMed
64.
go back to reference Duijvesz D, Luider T, Bangma CH, Jenster G. Exosomes as biomarker treasure chests for prostate cancer. Eur Urol. 2011;59:823–31.CrossRefPubMed Duijvesz D, Luider T, Bangma CH, Jenster G. Exosomes as biomarker treasure chests for prostate cancer. Eur Urol. 2011;59:823–31.CrossRefPubMed
65.
go back to reference Bryant RJ, Pawlowski T, Catto JW, Marsden G, Vessella RL, Rhees B, et al. Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer. 2012;106:768–74.CrossRefPubMedCentralPubMed Bryant RJ, Pawlowski T, Catto JW, Marsden G, Vessella RL, Rhees B, et al. Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer. 2012;106:768–74.CrossRefPubMedCentralPubMed
66.
go back to reference Santiago-Dieppa DR, Steinberg J, Gonda D, Cheung VJ, Carter BS, Chen CC. Extracellular vesicles as a platform for ‘liquid biopsy’ in glioblastoma patients. Expert Rev Mol Diagn. 2014;14:819–25.CrossRefPubMed Santiago-Dieppa DR, Steinberg J, Gonda D, Cheung VJ, Carter BS, Chen CC. Extracellular vesicles as a platform for ‘liquid biopsy’ in glioblastoma patients. Expert Rev Mol Diagn. 2014;14:819–25.CrossRefPubMed
67.
go back to reference Alegre E, Sanmamed MF, Rodriguez C, Carranza O, Martin-Algarra S, Gonzalez A. Study of circulating microRNA-125b levels in serum exosomes in advanced melanoma. Arch Pathol Lab Med. 2014;138:828–32.CrossRefPubMed Alegre E, Sanmamed MF, Rodriguez C, Carranza O, Martin-Algarra S, Gonzalez A. Study of circulating microRNA-125b levels in serum exosomes in advanced melanoma. Arch Pathol Lab Med. 2014;138:828–32.CrossRefPubMed
68.
go back to reference Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology. 2011;54:1237–48.CrossRefPubMedCentralPubMed Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology. 2011;54:1237–48.CrossRefPubMedCentralPubMed
69.
go back to reference Wang W, Li H, Zhou Y, Jie S. Peripheral blood microvesicles are potential biomarkers for hepatocellular carcinoma. Cancer Biomarkers. 2013;13:351–7.PubMed Wang W, Li H, Zhou Y, Jie S. Peripheral blood microvesicles are potential biomarkers for hepatocellular carcinoma. Cancer Biomarkers. 2013;13:351–7.PubMed
70.
go back to reference Baran J, Baj-Krzyworzeka M, Weglarczyk K, Szatanek R, Zembala M, Barbasz J, et al. Circulating tumour-derived microvesicles in plasma of gastric cancer patients. Cancer Immunol, Immunother. 2010;59:841–50.CrossRef Baran J, Baj-Krzyworzeka M, Weglarczyk K, Szatanek R, Zembala M, Barbasz J, et al. Circulating tumour-derived microvesicles in plasma of gastric cancer patients. Cancer Immunol, Immunother. 2010;59:841–50.CrossRef
71.
go back to reference Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008;110:13–21.CrossRefPubMed Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008;110:13–21.CrossRefPubMed
73.
go back to reference Corcoran C, Friel AM, Duffy MJ, Crown J, O’Driscoll L. Intracellular and extracellular microRNAs in breast cancer. Clin Chem. 2011;57:18–32.CrossRefPubMed Corcoran C, Friel AM, Duffy MJ, Crown J, O’Driscoll L. Intracellular and extracellular microRNAs in breast cancer. Clin Chem. 2011;57:18–32.CrossRefPubMed
74.
go back to reference Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer. 2009;10:42–6.CrossRefPubMed Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer. 2009;10:42–6.CrossRefPubMed
75.
go back to reference Rosell R, Wei J, Taron M. Circulating microRNA signatures of tumor-derived exosomes for early diagnosis of non-small-cell lung cancer. Clin Lung Cancer. 2009;10:8–9.CrossRefPubMed Rosell R, Wei J, Taron M. Circulating microRNA signatures of tumor-derived exosomes for early diagnosis of non-small-cell lung cancer. Clin Lung Cancer. 2009;10:8–9.CrossRefPubMed
76.
go back to reference Miller IV, Raposo G, Welsch U, da Prazeres CO, Thiel U, Lebar M, et al. First identification of Ewing’s sarcoma-derived extracellular vesicles and exploration of their biological and potential diagnostic implications. Biol Cell. 2013;105:289–303.CrossRefPubMed Miller IV, Raposo G, Welsch U, da Prazeres CO, Thiel U, Lebar M, et al. First identification of Ewing’s sarcoma-derived extracellular vesicles and exploration of their biological and potential diagnostic implications. Biol Cell. 2013;105:289–303.CrossRefPubMed
77.
go back to reference Yamada T, Shigemura H, Ishiguro N, Inoshima Y. Cell Infectivity in relation to bovine leukemia virus gp51 and p24 in bovine milk exosomes. PLoS ONE. 2013;8:e77359.CrossRefPubMedCentralPubMed Yamada T, Shigemura H, Ishiguro N, Inoshima Y. Cell Infectivity in relation to bovine leukemia virus gp51 and p24 in bovine milk exosomes. PLoS ONE. 2013;8:e77359.CrossRefPubMedCentralPubMed
78.
go back to reference Zhu X, You Y, Li Q, Zeng C, Fu F, Guo A, et al. BCR-ABL1-positive microvesicles transform normal hematopoietic transplants through genomic instability: implications for donor cell leukemia. Leukemia. 2014;28:1666–75.CrossRefPubMed Zhu X, You Y, Li Q, Zeng C, Fu F, Guo A, et al. BCR-ABL1-positive microvesicles transform normal hematopoietic transplants through genomic instability: implications for donor cell leukemia. Leukemia. 2014;28:1666–75.CrossRefPubMed
79.
go back to reference Zheng F, Li J, Du W, Wang N, Li H, Huang S. Human ether-a-go-go-related gene K+ channels regulate shedding of leukemia cell-derived microvesicles. Leukemia & Lymphoma. 2012;53:1592–8.CrossRef Zheng F, Li J, Du W, Wang N, Li H, Huang S. Human ether-a-go-go-related gene K+ channels regulate shedding of leukemia cell-derived microvesicles. Leukemia & Lymphoma. 2012;53:1592–8.CrossRef
80.
go back to reference Domnikova NP, Dolgikh TY, Sholenberg EV, Vorontsova EV, Goreva OB, Mel’nikova EV, et al. Blood microvesicles during chronic lymphoproliferative diseases. Bull Exp Biol Med. 2013;156:94–7.CrossRefPubMed Domnikova NP, Dolgikh TY, Sholenberg EV, Vorontsova EV, Goreva OB, Mel’nikova EV, et al. Blood microvesicles during chronic lymphoproliferative diseases. Bull Exp Biol Med. 2013;156:94–7.CrossRefPubMed
81.
go back to reference Szczepanski MJ, Szajnik M, Welsh A, Whiteside TL, Boyiadzis M. Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-beta1. Haematologica. 2011;96:1302–9.CrossRefPubMedCentralPubMed Szczepanski MJ, Szajnik M, Welsh A, Whiteside TL, Boyiadzis M. Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-beta1. Haematologica. 2011;96:1302–9.CrossRefPubMedCentralPubMed
82.
go back to reference Hedlund M, Nagaeva O, Kargl D, Baranov V, Mincheva-Nilsson L. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS ONE. 2011;6:e16899.CrossRefPubMedCentralPubMed Hedlund M, Nagaeva O, Kargl D, Baranov V, Mincheva-Nilsson L. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS ONE. 2011;6:e16899.CrossRefPubMedCentralPubMed
83.
go back to reference Ratajczak MZ, Kucia M, Jadczyk T, Greco NJ, Wojakowski W, Tendera M, et al. Pivotal role of paracrine effects in stem cell therapies in regenerative medicine: can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies? Leukemia. 2012;26:1166–73.CrossRefPubMed Ratajczak MZ, Kucia M, Jadczyk T, Greco NJ, Wojakowski W, Tendera M, et al. Pivotal role of paracrine effects in stem cell therapies in regenerative medicine: can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies? Leukemia. 2012;26:1166–73.CrossRefPubMed
84.
go back to reference Di Noto G, Paolini L, Zendrini A, Radeghieri A, Caimi L, Ricotta D. C-src enriched serum microvesicles are generated in malignant plasma cell dyscrasia. PLoS ONE. 2013;8:e70811.CrossRefPubMedCentralPubMed Di Noto G, Paolini L, Zendrini A, Radeghieri A, Caimi L, Ricotta D. C-src enriched serum microvesicles are generated in malignant plasma cell dyscrasia. PLoS ONE. 2013;8:e70811.CrossRefPubMedCentralPubMed
85.
go back to reference Mineo M, Garfield SH, Taverna S, Flugy A, De Leo G, Alessandro R, et al. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion. Angiogenesis. 2012;15:33–45.CrossRefPubMedCentralPubMed Mineo M, Garfield SH, Taverna S, Flugy A, De Leo G, Alessandro R, et al. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion. Angiogenesis. 2012;15:33–45.CrossRefPubMedCentralPubMed
86.
go back to reference Liu Y, Zhu XJ, Zeng C, Wu PH, Wang HX, Chen ZC, et al. Microvesicles secreted from human multiple myeloma cells promote angiogenesis. Acta Pharmacol Sin. 2014;35:230–8.CrossRefPubMed Liu Y, Zhu XJ, Zeng C, Wu PH, Wang HX, Chen ZC, et al. Microvesicles secreted from human multiple myeloma cells promote angiogenesis. Acta Pharmacol Sin. 2014;35:230–8.CrossRefPubMed
87.
go back to reference Arendt BK, Walters DK, Wu X, Tschumper RC, Jelinek DF. Multiple myeloma dell-derived microvesicles are enriched in CD147 expression and enhance tumor cell proliferation. Oncotarget. 2014;5:5686–99.PubMedCentralPubMed Arendt BK, Walters DK, Wu X, Tschumper RC, Jelinek DF. Multiple myeloma dell-derived microvesicles are enriched in CD147 expression and enhance tumor cell proliferation. Oncotarget. 2014;5:5686–99.PubMedCentralPubMed
88.
go back to reference Sun L, Wang HX, Zhu XJ, Wu PH, Chen WQ, Zou P, et al. Serum deprivation elevates the levels of microvesicles with different size distributions and selectively enriched proteins in human myeloma cells in vitro. Acta Pharmacol Sin. 2014;35:381–93.CrossRefPubMed Sun L, Wang HX, Zhu XJ, Wu PH, Chen WQ, Zou P, et al. Serum deprivation elevates the levels of microvesicles with different size distributions and selectively enriched proteins in human myeloma cells in vitro. Acta Pharmacol Sin. 2014;35:381–93.CrossRefPubMed
89.
go back to reference Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS ONE. 2010;5:e13247.CrossRefPubMedCentralPubMed Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS ONE. 2010;5:e13247.CrossRefPubMedCentralPubMed
90.
go back to reference Umezu T, Ohyashiki K, Kuroda M, Ohyashiki JH. Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene. 2013;32:2747–55.CrossRefPubMed Umezu T, Ohyashiki K, Kuroda M, Ohyashiki JH. Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene. 2013;32:2747–55.CrossRefPubMed
91.
go back to reference 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;288:34343–51.CrossRefPubMedCentralPubMed 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;288:34343–51.CrossRefPubMedCentralPubMed
92.
go back to reference Roccaro AM, Sacco A, Maiso P, Azab AK, Tai YT, Reagan M, et al. BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest. 2013;123:1542–55.CrossRefPubMedCentralPubMed Roccaro AM, Sacco A, Maiso P, Azab AK, Tai YT, Reagan M, et al. BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest. 2013;123:1542–55.CrossRefPubMedCentralPubMed
93.
go back to reference Wang J, Hendrix A, Hernot S, Lemaire M, De Bruyne E, Van Valckenborgh E, et al. Bone marrow stromal cell-derived exosomes as communicators in drug resistance in multiple myeloma cells. Blood. 2014;124:555–66.CrossRefPubMed Wang J, Hendrix A, Hernot S, Lemaire M, De Bruyne E, Van Valckenborgh E, et al. Bone marrow stromal cell-derived exosomes as communicators in drug resistance in multiple myeloma cells. Blood. 2014;124:555–66.CrossRefPubMed
94.
go back to reference Luga V, Wrana JL. Tumor-stroma interaction: revealing fibroblast-secreted exosomes as potent regulators of Wnt-planar cell polarity signaling in cancer metastasis. Cancer Res. 2013;73:6843–7.CrossRefPubMed Luga V, Wrana JL. Tumor-stroma interaction: revealing fibroblast-secreted exosomes as potent regulators of Wnt-planar cell polarity signaling in cancer metastasis. Cancer Res. 2013;73:6843–7.CrossRefPubMed
95.
go back to reference Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998;4:594–600.CrossRefPubMed Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998;4:594–600.CrossRefPubMed
96.
go back to reference Gastpar R, Gehrmann M, Bausero MA, Asea A, Gross C, Schroeder JA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 2005;65:5238–47.CrossRefPubMedCentralPubMed Gastpar R, Gehrmann M, Bausero MA, Asea A, Gross C, Schroeder JA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 2005;65:5238–47.CrossRefPubMedCentralPubMed
Metadata
Title
Transfer of microRNAs by extracellular membrane microvesicles: a nascent crosstalk model in tumor pathogenesis, especially tumor cell-microenvironment interactions
Authors
Li Zhang
C Alexander Valencia
Biao Dong
Meng Chen
Pu-Jun Guan
Ling Pan
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Journal of Hematology & Oncology / Issue 1/2015
Electronic ISSN: 1756-8722
DOI
https://doi.org/10.1186/s13045-015-0111-y

Other articles of this Issue 1/2015

Journal of Hematology & Oncology 1/2015 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine