Cell-to-cell miRNA transfer: From body homeostasis to therapy

Pharmacology and Therapeutics

Volumn 136, Issue 2, 2012, Pages 169-174

  Redis, Roxana S ^a,b   Calin, Steliana ^a   Yang, Yaling ^a   You, M James ^a,c   Calin, George A ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b IULIU HATIEGANU UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

Body fluids; HGT; Hormones; miRNAs; Nanovesicles; Therapy

Indexed keywords

HORMONE; MICRORNA; MICRORNA 124A; MICRORNA 125B; MICRORNA 150; MICRORNA 155; MICRORNA 15A; MICRORNA 16; MICRORNA 17; MICRORNA 19B; MICRORNA 20A; MICRORNA 223; MICRORNA 26A; MICRORNA 29B; MICRORNA 451; MICRORNA 709; MICRORNA 92; UNCLASSIFIED DRUG;

BODY FLUID; CELL COMMUNICATION; CELL TRANSFER; CLINICAL PRACTICE; EXPRESSION VECTOR; GENE OVEREXPRESSION; GENE TARGETING; GENE TRANSFER; HOMEOSTASIS; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA TRANSLATION; RNA TRANSPORT; TUMOR MICROENVIRONMENT;

ANIMALS; CELL COMMUNICATION; GENE TRANSFER, HORIZONTAL; HOMEOSTASIS; HUMANS; MICRORNAS; TUMOR MICROENVIRONMENT;

EID: 84867334962     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2012.08.003     Document Type: Review

References (72)

1. X. Agirre, A. Vilas-Zornoza, A. Jimenez-Velasco, J.I. Martin-Subero, L. Cordeu, L. Garate, E. San Jose-Eneriz, G. Abizanda, P. Rodriguez-Otero, P. Fortes, J. Rifon, E. Bandres, M.J. Calasanz, V. Martin, A. Heiniger, A. Torres, R. Siebert, J. Roman-Gomez, and F. Prosper Epigenetic silencing of the tumor suppressor microRNA Hsa-miR-124a regulates CDK6 expression and confers a poor prognosis in acute lymphoblastic leukemia Cancer Res 69 2009 4443 4453
2. K.A. Ahmed, and J. Xiang Mechanisms of cellular communication through intercellular protein transfer J Cell Mol Med 15 2011 1458 1473
3. V. Ambros MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing Cell 113 2003 673 676
4. J.D. Arroyo, J.R. Chevillet, E.M. Kroh, I.K. Ruf, C.C. Pritchard, D.F. Gibson, P.S. Mitchell, C.F. Bennett, E.L. Pogosova-Agadjanyan, D.L. Stirewalt, J.F. Tait, and M. Tewari Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma Proc Natl Acad Sci U S A 108 2011 5003 5008
5. M. Babst A protein's final ESCRT Traffic 6 2005 2 9
6. M. Boeri, C. Verri, D. Conte, L. Roz, P. Modena, F. Facchinetti, E. Calabro, C.M. Croce, U. Pastorino, and G. Sozzi MicroRNA signatures in tissues and plasma predict development and prognosis of computed tomography detected lung cancer Proc Natl Acad Sci U S A 108 2011 3713 3718
7. M. Bousquet, M.H. Harris, B. Zhou, and H.F. Lodish MicroRNA miR-125b causes leukemia Proc Natl Acad Sci U S A 107 2010 21558 21563
8. G.A. Calin, A. Cimmino, M. Fabbri, M. Ferracin, S.E. Wojcik, M. Shimizu, C. Taccioli, N. Zanesi, R. Garzon, R.I. Aqeilan, H. Alder, S. Volinia, L. Rassenti, X. Liu, C.G. Liu, T.J. Kipps, M. Negrini, and C.M. Croce MiR-15a and miR-16-1 cluster functions in human leukemia Proc Natl Acad Sci U S A 105 2008 5166 5171
9. G.A. Calin, C.D. Dumitru, M. Shimizu, R. Bichi, S. Zupo, E. Noch, H. Aldler, S. Rattan, M. Keating, K. Rai, L. Rassenti, T. Kipps, M. Negrini, F. Bullrich, and C.M. Croce Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia Proc Natl Acad Sci U S A 99 2002 15524 15529
10. X. Chen, Y. Ba, L. Ma, X. Cai, Y. Yin, K. Wang, J. Guo, Y. Zhang, J. Chen, X. Guo, Q. Li, X. Li, W. Wang, J. Wang, X. Jiang, Y. Xiang, C. Xu, P. Zheng, J. Zhang, R. Li, H. Zhang, X. Shang, T. Gong, G. Ning, K. Zen, and C.Y. Zhang Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases Cell Res 18 2008 997 1006
11. V. Ciravolo, V. Huber, G.C. Ghedini, E. Venturelli, F. Bianchi, M. Campiglio, D. Morelli, A. Villa, P. Della Mina, S. Menard, P. Filipazzi, L. Rivoltini, E. Tagliabue, and S.M. Pupa Potential role of HER2-overexpressing exosomes in countering trastuzumab-based therapy J Cell Physiol 227 2012 658 667
12. E. Cocucci, G. Racchetti, and J. Meldolesi Shedding microvesicles: artefacts no more Trends Cell Biol 19 2009 43 51
13. E. Cocucci, G. Racchetti, P. Podini, and J. Meldolesi Enlargeosome traffic: exocytosis triggered by various signals is followed by endocytosis, membrane shedding or both Traffic 8 2007 742 757
14. F. Collino, M.C. Deregibus, S. Bruno, L. Sterpone, G. Aghemo, L. Viltono, C. Tetta, and G. Camussi Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs PLoS One 5 2010 e11803
15. S. Costinean, N. Zanesi, Y. Pekarsky, E. Tili, S. Volinia, N. Heerema, and C.M. Croce Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice Proc Natl Acad Sci U S A 103 2006 7024 7029
16. J.C. da Silveira, D.N. Veeramachaneni, Q.A. Winger, E.M. Carnevale, and G.J. Bouma Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle Biol Reprod 86 2012 71
17. S. Fichtlscherer, S. De Rosa, H. Fox, T. Schwietz, A. Fischer, C. Liebetrau, M. Weber, C.W. Hamm, T. Roxe, M. Muller-Ardogan, A. Bonauer, A.M. Zeiher, and S. Dimmeler Circulating microRNAs in patients with coronary artery disease Circ Res 107 2010 677 684
18. R. Garzon, C.E. Heaphy, V. Havelange, M. Fabbri, S. Volinia, T. Tsao, N. Zanesi, S.M. Kornblau, G. Marcucci, G.A. Calin, M. Andreeff, and C.M. Croce MicroRNA 29b functions in acute myeloid leukemia Blood 114 2009 5331 5341
19. O. Gasser, C. Hess, S. Miot, C. Deon, J.C. Sanchez, and J.A. Schifferli Characterisation and properties of ectosomes released by human polymorphonuclear neutrophils Exp Cell Res 285 2003 243 257
20. D.J. Gibbings, C. Ciaudo, M. Erhardt, and O. Voinnet Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity Nat Cell Biol 11 2009 1143 1149
21. I. Giusti, S. D'Ascenzo, D. Millimaggi, G. Taraboletti, G. Carta, N. Franceschini, A. Pavan, and V. Dolo Cathepsin B mediates the pH-dependent proinvasive activity of tumor-shed microvesicles Neoplasia 10 2008 481 488
22. C. Gourzones, A. Gelin, I. Bombik, J. Klibi, B. Verillaud, J. Guigay, P. Lang, S. Temam, V. Schneider, C. Amiel, S. Baconnais, A.S. Jimenez, and P. Busson Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells Virol J 7 2010 271
23. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
24. L. He, and G.J. Hannon MicroRNAs: small RNAs with a big role in gene regulation Nat Rev Genet 5 2004 522 531
25. K. Hede Looking at cancer through an evolutionary lens J Natl Cancer Inst 101 2009 1108 1109
26. M. Hedlund, O. Nagaeva, D. Kargl, V. Baranov, and L. Mincheva-Nilsson Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells PLoS One 6 2011 e16899
27. Z. Hu, X. Chen, Y. Zhao, T. Tian, G. Jin, Y. Shu, Y. Chen, L. Xu, K. Zen, C. Zhang, and H. Shen Serum microRNA signatures identified in a genome-wide serum microRNA expression profiling predict survival of non-small-cell lung cancer J Clin Oncol 28 2010 1721 1726
28. M. Hu, and K. Polyak Molecular characterisation of the tumour microenvironment in breast cancer Eur J Cancer 44 2008 2760 2765
29. Z. Huang, D. Huang, S. Ni, Z. Peng, W. Sheng, and X. Du Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer Int J Cancer 127 2010 118 126
30. M.P. Hunter, N. Ismail, X. Zhang, B.D. Aguda, E.J. Lee, L. Yu, T. Xiao, J. Schafer, M.L. Lee, T.D. Schmittgen, S.P. Nana-Sinkam, D. Jarjoura, and C.B. Marsh Detection of microRNA expression in human peripheral blood microvesicles PLoS One 3 2008 e3694
31. E.J. Jung, L. Santarpia, J. Kim, F.J. Esteva, E. Moretti, A.U. Buzdar, A. Di Leo, X.F. Le, R.C. Bast Jr., S.T. Park, L. Pusztai, and G.A. Calin Plasma microRNA 210 levels correlate with sensitivity to trastuzumab and tumor presence in breast cancer patients Cancer 118 2012 2603 2614
32. R.N. Kaplan, R.D. Riba, S. Zacharoulis, A.H. Bramley, L. Vincent, C. Costa, D.D. MacDonald, D.K. Jin, K. Shido, S.A. Kerns, Z. Zhu, D. Hicklin, Y. Wu, J.L. Port, N. Altorki, E.R. Port, D. Ruggero, S.V. Shmelkov, K.K. Jensen, S. Rafii, and D. Lyden VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche Nature 438 2005 820 827
33. S. Khan, J.M. Jutzy, J.R. Aspe, D.W. McGregor, J.W. Neidigh, and N.R. Wall Survivin is released from cancer cells via exosomes Apoptosis 16 2011 1 12
34. V.N. Kim MicroRNA biogenesis: coordinated cropping and dicing Nat Rev Mol Cell Biol 6 2005 376 385
35. N. Kosaka, H. Iguchi, Y. Yoshioka, F. Takeshita, Y. Matsuki, and T. Ochiya Secretory mechanisms and intercellular transfer of microRNAs in living cells J Biol Chem 285 2010 17442 17452
36. N. Kosaka, H. Izumi, K. Sekine, and T. Ochiya microRNA as a new immune-regulatory agent in breast milk Silence 1 2010 7
37. J.S. Lawson, W.K. Glenn, B. Salmons, Y. Ye, B. Heng, P. Moody, H. Johal, W.D. Rawlinson, W. Delprado, L. Lutze-Mann, and N.J. Whitaker Mouse mammary tumor virus-like sequences in human breast cancer Cancer Res 70 2010 3576 3585
38. X.Y. Li, T. Sanda, A.T. Look, C.D. Novina, and H. von Boehmer Repression of tumor suppressor miR-451 is essential for NOTCH1-induced oncogenesis in T-ALL J Exp Med 208 2011 663 675
39. G. Majno, and I. Joris Apoptosis, oncosis, and necrosis. An overview of cell death Am J Pathol 146 1995 3 15
40. M. Marsh, and G. van Meer Cell biology. No ESCRTs for exosomes Science 319 2008 1191 1192
41. S. Mathivanan, H. Ji, and R.J. Simpson Exosomes: extracellular organelles important in intercellular communication J Proteomics 73 2010 1907 1920
42. K.J. Mavrakis, J. Van Der Meulen, A.L. Wolfe, X. Liu, E. Mets, T. Taghon, A.A. Khan, M. Setty, P. Rondou, P. Vandenberghe, E. Delabesse, Y. Benoit, N.B. Socci, C.S. Leslie, P. Van Vlierberghe, F. Speleman, and H.G. Wendel A cooperative microRNA-tumor suppressor gene network in acute T-cell lymphoblastic leukemia (T-ALL) Nat Genet 43 2011 673 678
43. L. Mincheva-Nilsson, and V. Baranov The role of placental exosomes in reproduction Am J Reprod Immunol 63 2010 520 533
44. P.S. Mitchell, R.K. Parkin, E.M. Kroh, B.R. Fritz, S.K. Wyman, E.L. Pogosova-Agadjanyan, A. Peterson, J. Noteboom, K.C. O'Briant, A. Allen, D.W. Lin, N. Urban, C.W. Drescher, B.S. Knudsen, D.L. Stirewalt, R. Gentleman, R.L. Vessella, P.S. Nelson, D.B. Martin, and M. Tewari Circulating microRNAs as stable blood-based markers for cancer detection Proc Natl Acad Sci U S A 105 2008 10513 10518
45. M. Mittelbrunn, C. Gutierrez-Vazquez, C. Villarroya-Beltri, S. Gonzalez, F. Sanchez-Cabo, M.A. Gonzalez, A. Bernad, and F. Sanchez-Madrid Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells Nat Commun 2 2011 282
46. S. Mochizuki, and Y. Okada ADAMs in cancer cell proliferation and progression Cancer Sci 98 2007 621 628
47. A. Montecalvo, A.T. Larregina, W.J. Shufesky, D.B. Stolz, M.L. Sullivan, J.M. Karlsson, C.J. Baty, G.A. Gibson, G. Erdos, Z. Wang, J. Milosevic, O.A. Tkacheva, S.J. Divito, R. Jordan, J. Lyons-Weiler, S.C. Watkins, and A.E. Morelli Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes Blood 119 2012 756 766
48. K. Ohshima, K. Inoue, A. Fujiwara, K. Hatakeyama, K. Kanto, Y. Watanabe, K. Muramatsu, Y. Fukuda, S. Ogura, K. Yamaguchi, and T. Mochizuki Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line PLoS One 5 2010 e13247
49. I. Parolini, C. Federici, C. Raggi, L. Lugini, S. Palleschi, A. De Milito, C. Coscia, E. Iessi, M. Logozzi, A. Molinari, M. Colone, M. Tatti, M. Sargiacomo, and S. Fais Microenvironmental pH is a key factor for exosome traffic in tumor cells J Biol Chem 284 2009 34211 34222
50. D.M. Pegtel, K. Cosmopoulos, D.A. Thorley-Lawson, M.A. van Eijndhoven, E.S. Hopmans, J.L. Lindenberg, T.D. de Gruijl, T. Wurdinger, and J.M. Middeldorp Functional delivery of viral miRNAs via exosomes Proc Natl Acad Sci U S A 107 2010 6328 6333
51. H.J. Peltier, and G.J. Latham Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues RNA 14 2008 844 852
52. G. Rabinowits, C. Gercel-Taylor, J.M. Day, D.D. Taylor, and G.H. Kloecker Exosomal microRNA: a diagnostic marker for lung cancer Clin Lung Cancer 10 2009 42 46
53. J. Ratajczak, K. Miekus, M. Kucia, J. Zhang, R. Reca, P. Dvorak, and M.Z. Ratajczak Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery Leukemia 20 2006 847 856
54. B.J. Scaglione, E. Salerno, M. Balan, F. Coffman, P. Landgraf, F. Abbasi, S. Kotenko, G.E. Marti, and E.S. Raveche Murine models of chronic lymphocytic leukaemia: role of microRNA-16 in the New Zealand Black mouse model Br J Haematol 139 2007 645 657
55. M. Simons, and G. Raposo Exosomes - vesicular carriers for intercellular communication Curr Opin Cell Biol 21 2009 575 581
56. J. Skog, T. Wurdinger, S. van Rijn, D.H. Meijer, L. Gainche, M. Sena-Esteves, W.T. Curry Jr., B.S. Carter, A.M. Krichevsky, and X.O. Breakefield Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers Nat Cell Biol 10 2008 1470 1476
57. N. Tano, H.W. Kim, and M. Ashraf microRNA-150 regulates mobilization and migration of bone marrow-derived mononuclear cells by targeting Cxcr4 PLoS One 6 2011 e23114
58. D.D. Taylor, and C. Gercel-Taylor MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer Gynecol Oncol 110 2008 13 21
59. C. Thery, L. Zitvogel, and S. Amigorena Exosomes: composition, biogenesis and function Nat Rev Immunol 2 2002 569 579
60. K. Trajkovic, C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brugger, and M. Simons Ceramide triggers budding of exosome vesicles into multivesicular endosomes Science 319 2008 1244 1247
61. A. Turchinovich, L. Weiz, A. Langheinz, and B. Burwinkel Characterization of extracellular circulating microRNA Nucleic Acids Res 39 2011 7223 7233
62. H. Valadi, K. Ekstrom, A. Bossios, M. Sjostrand, J.J. Lee, and J.O. Lotvall Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat Cell Biol 9 2007 654 659
63. S. Vasudevan, Y. Tong, and J.A. Steitz Switching from repression to activation: microRNAs can up-regulate translation Science 318 2007 1931 1934
64. K.C. Vickers, B.T. Palmisano, B.M. Shoucri, R.D. Shamburek, and A.T. Remaley MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins Nat Cell Biol 13 2011 423 433
65. K. Wang, S. Zhang, J. Weber, D. Baxter, and D.J. Galas Export of microRNAs and microRNA-protective protein by mammalian cells Nucleic Acids Res 38 2010 7248 7259
66. G.J. Weiss, L.T. Bemis, E. Nakajima, M. Sugita, D.K. Birks, W.A. Robinson, M. Varella-Garcia, P.A. Bunn Jr., J. Haney, B.A. Helfrich, H. Kato, F.R. Hirsch, and W.A. Franklin EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell lines Ann Oncol 19 2008 1053 1059
67. M. Yang, J. Chen, F. Su, B. Yu, L. Lin, Y. Liu, J.D. Huang, and E. Song Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells Mol Cancer 10 2011 117
68. A. Zampetaki, S. Kiechl, I. Drozdov, P. Willeit, U. Mayr, M. Prokopi, A. Mayr, S. Weger, F. Oberhollenzer, E. Bonora, A. Shah, J. Willeit, and M. Mayr Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes Circ Res 107 2010 810 817
69. A. Zernecke, K. Bidzhekov, H. Noels, E. Shagdarsuren, L. Gan, B. Denecke, M. Hristov, T. Koppel, M.N. Jahantigh, E. Lutgens, S. Wang, E.N. Olson, A. Schober, and C. Weber Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection Sci Signal 2 2009 ra81
70. L. Zhang, D. Hou, X. Chen, D. Li, L. Zhu, Y. Zhang, J. Li, Z. Bian, X. Liang, X. Cai, Y. Yin, C. Wang, T. Zhang, D. Zhu, D. Zhang, J. Xu, Q. Chen, Y. Ba, J. Liu, Q. Wang, J. Chen, J. Wang, M. Wang, Q. Zhang, J. Zhang, K. Zen, and C.Y. Zhang Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA Cell Res 22 2012 107 126
71. Y. Zhang, D. Liu, X. Chen, J. Li, L. Li, Z. Bian, F. Sun, J. Lu, Y. Yin, X. Cai, Q. Sun, K. Wang, Y. Ba, Q. Wang, D. Wang, J. Yang, P. Liu, T. Xu, Q. Yan, J. Zhang, K. Zen, and C.Y. Zhang Secreted monocytic miR-150 enhances targeted endothelial cell migration Mol Cell 39 2010 133 144
72. Q. Zhou, M. Li, X. Wang, Q. Li, T. Wang, Q. Zhu, X. Zhou, X. Gao, and X. Li Immune-related microRNAs are abundant in breast milk exosomes Int J Biol Sci 8 2012 118 123