Home LiteratureArticle Details
PMID: 22903157 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Cell-to-cell miRNA transfer: from body homeostasis to therapy.

Pharmacology & therapeutics ·Vol. 136 ·No. 2 ·2012-11-00 ·Pages 169-74

Redis RS, Calin S, Yang Y, You MJ, Calin GA

Abstract

The role of non-protein coding RNAs (ncRNAs), microRNAs (miRNAs) in particular, as fine-tuners of both pathological and physiological processes is no longer a matter of debate. With the recent discovery of miRNAs in a wide variety of body fluids and considering them as tools employed in horizontal gene transfer between cells, a new horizon opens in the field of diagnosis and therapeutics. Circulating miRNAs not only enable the communication among cells, but also provide insight into the pathological and physiological state of the originating cells. In this review we summarize the recent advances made in this field, arguing for compelling translation of miRNAs into clinical practice. Moreover, we provide overview of their characteristics and how they impact the evolution of tumor microenvironment and cell-to-cell communication, advancing the idea that miRNAs may function as hormones.

MeSH Terms
Animals Cell Communication Gene Transfer, Horizontal Homeostasis Humans MicroRNAs/blood,genetics,metabolism Tumor Microenvironment
Chemicals
MicroRNAs
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Redis Roxana S
Department of Experimental Therapeutics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Calin Steliana
Yang Yaling
You M James
Calin George A
References (72)
72 references, click to expand
  1. Exosomes: composition, biogenesis and function.
    Nat Rev Immunol. 2002 Aug;2(8):569-79 PMID: 12154376
  2. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs.
    PLoS One. 2010 Jul 27;5(7):e11803 PMID: 20668554
  3. Shedding microvesicles: artefacts no more.
    Trends Cell Biol. 2009 Feb;19(2):43-51 PMID: 19144520
  4. Murine models of chronic lymphocytic leukaemia: role of microRNA-16 in the New Zealand Black mouse model.
    Br J Haematol. 2007 Dec;139(5):645-57 PMID: 17941951
  5. 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. 2012 Mar 19;86(3):71 PMID: 22116803
  6. MicroRNA miR-125b causes leukemia.
    Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21558-63 PMID: 21118985
  7. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells.
    PLoS One. 2011 Feb 25;6(2):e16899 PMID: 21364924
  8. Apoptosis, oncosis, and necrosis. An overview of cell death.
    Am J Pathol. 1995 Jan;146(1):3-15 PMID: 7856735
  9. Enlargeosome traffic: exocytosis triggered by various signals is followed by endocytosis, membrane shedding or both.
    Traffic. 2007 Jun;8(6):742-57 PMID: 17488290
  10. Exosomal microRNA: a diagnostic marker for lung cancer.
    Clin Lung Cancer. 2009 Jan;10(1):42-6 PMID: 19289371
  11. Serum microRNA signatures identified in a genome-wide serum microRNA expression profiling predict survival of non-small-cell lung cancer.
    J Clin Oncol. 2010 Apr 1;28(10):1721-6 PMID: 20194856
  12. Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice.
    Proc Natl Acad Sci U S A. 2006 May 2;103(18):7024-9 PMID: 16641092
  13. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes.
    Blood. 2012 Jan 19;119(3):756-66 PMID: 22031862
  14. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers.
    Nat Cell Biol. 2008 Dec;10(12):1470-6 PMID: 19011622
  15. Hallmarks of cancer: the next generation.
    Cell. 2011 Mar 4;144(5):646-74 PMID: 21376230
  16. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity.
    Nat Cell Biol. 2009 Sep;11(9):1143-9 PMID: 19684575
  17. Circulating microRNAs in patients with coronary artery disease.
    Circ Res. 2010 Sep 3;107(5):677-84 PMID: 20595655
  18. A cooperative microRNA-tumor suppressor gene network in acute T-cell lymphoblastic leukemia (T-ALL).
    Nat Genet. 2011 Jun 05;43(7):673-8 PMID: 21642990
  19. Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer.
    Int J Cancer. 2010 Jul 1;127(1):118-26 PMID: 19876917
  20. Mouse mammary tumor virus-like sequences in human breast cancer.
    Cancer Res. 2010 May 1;70(9):3576-85 PMID: 20388779
  21. Plasma microRNA 210 levels correlate with sensitivity to trastuzumab and tumor presence in breast cancer patients.
    Cancer. 2012 May 15;118(10):2603-14 PMID: 22370716
  22. ADAMs in cancer cell proliferation and progression.
    Cancer Sci. 2007 May;98(5):621-8 PMID: 17355265
  23. MicroRNA 29b functions in acute myeloid leukemia.
    Blood. 2009 Dec 17;114(26):5331-41 PMID: 19850741
  24. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins.
    Nat Cell Biol. 2011 Apr;13(4):423-33 PMID: 21423178
  25. Ceramide triggers budding of exosome vesicles into multivesicular endosomes.
    Science. 2008 Feb 29;319(5867):1244-7 PMID: 18309083
  26. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma.
    Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):5003-8 PMID: 21383194
  27. Epigenetic silencing of the tumor suppressor microRNA Hsa-miR-124a regulates CDK6 expression and confers a poor prognosis in acute lymphoblastic leukemia.
    Cancer Res. 2009 May 15;69(10):4443-53 PMID: 19435910
  28. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA.
    Cell Res. 2012 Jan;22(1):107-26 PMID: 21931358
  29. microRNA as a new immune-regulatory agent in breast milk.
    Silence. 2010 Mar 01;1(1):7 PMID: 20226005
  30. Secretory mechanisms and intercellular transfer of microRNAs in living cells.
    J Biol Chem. 2010 Jun 4;285(23):17442-52 PMID: 20353945
  31. Cathepsin B mediates the pH-dependent proinvasive activity of tumor-shed microvesicles.
    Neoplasia. 2008 May;10(5):481-8 PMID: 18472965
  32. Survivin is released from cancer cells via exosomes.
    Apoptosis. 2011 Jan;16(1):1-12 PMID: 20717727
  33. Microenvironmental pH is a key factor for exosome traffic in tumor cells.
    J Biol Chem. 2009 Dec 4;284(49):34211-22 PMID: 19801663
  34. MicroRNA biogenesis: coordinated cropping and dicing.
    Nat Rev Mol Cell Biol. 2005 May;6(5):376-85 PMID: 15852042
  35. The role of placental exosomes in reproduction.
    Am J Reprod Immunol. 2010 Jun;63(6):520-33 PMID: 20331583
  36. Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells.
    Virol J. 2010 Oct 15;7:271 PMID: 20950422
  37. Cell biology. No ESCRTs for exosomes.
    Science. 2008 Feb 29;319(5867):1191-2 PMID: 18309064
  38. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche.
    Nature. 2005 Dec 8;438(7069):820-7 PMID: 16341007
  39. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer.
    Gynecol Oncol. 2008 Jul;110(1):13-21 PMID: 18589210
  40. MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing.
    Cell. 2003 Jun 13;113(6):673-6 PMID: 12809598
  41. MicroRNAs: small RNAs with a big role in gene regulation.
    Nat Rev Genet. 2004 Jul;5(7):522-31 PMID: 15211354
  42. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.
    Nat Cell Biol. 2007 Jun;9(6):654-9 PMID: 17486113
  43. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells.
    Mol Cancer. 2011 Sep 22;10:117 PMID: 21939504
  44. Functional delivery of viral miRNAs via exosomes.
    Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6328-33 PMID: 20304794
  45. MicroRNA signatures in tissues and plasma predict development and prognosis of computed tomography detected lung cancer.
    Proc Natl Acad Sci U S A. 2011 Mar 1;108(9):3713-8 PMID: 21300873
  46. Characterisation and properties of ectosomes released by human polymorphonuclear neutrophils.
    Exp Cell Res. 2003 May 1;285(2):243-57 PMID: 12706119
  47. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection.
    Sci Signal. 2009 Dec 08;2(100):ra81 PMID: 19996457
  48. Looking at cancer through an evolutionary lens.
    J Natl Cancer Inst. 2009 Aug 19;101(16):1108-9 PMID: 19671772
  49. 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. 2002 Nov 26;99(24):15524-9 PMID: 12434020
  50. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery.
    Leukemia. 2006 May;20(5):847-56 PMID: 16453000
  51. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases.
    Cell Res. 2008 Oct;18(10):997-1006 PMID: 18766170
  52. Immune-related microRNAs are abundant in breast milk exosomes.
    Int J Biol Sci. 2012;8(1):118-23 PMID: 22211110
  53. Switching from repression to activation: microRNAs can up-regulate translation.
    Science. 2007 Dec 21;318(5858):1931-4 PMID: 18048652
  54. Potential role of HER2-overexpressing exosomes in countering trastuzumab-based therapy.
    J Cell Physiol. 2012 Feb;227(2):658-67 PMID: 21465472
  55. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line.
    PLoS One. 2010 Oct 08;5(10):e13247 PMID: 20949044
  56. A protein's final ESCRT.
    Traffic. 2005 Jan;6(1):2-9 PMID: 15569240
  57. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes.
    Circ Res. 2010 Sep 17;107(6):810-7 PMID: 20651284
  58. Exosomes--vesicular carriers for intercellular communication.
    Curr Opin Cell Biol. 2009 Aug;21(4):575-81 PMID: 19442504
  59. Export of microRNAs and microRNA-protective protein by mammalian cells.
    Nucleic Acids Res. 2010 Nov;38(20):7248-59 PMID: 20615901
  60. Repression of tumor suppressor miR-451 is essential for NOTCH1-induced oncogenesis in T-ALL.
    J Exp Med. 2011 Apr 11;208(4):663-75 PMID: 21464222
  61. MiR-15a and miR-16-1 cluster functions in human leukemia.
    Proc Natl Acad Sci U S A. 2008 Apr 1;105(13):5166-71 PMID: 18362358
  62. Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues.
    RNA. 2008 May;14(5):844-52 PMID: 18375788
  63. Circulating microRNAs as stable blood-based markers for cancer detection.
    Proc Natl Acad Sci U S A. 2008 Jul 29;105(30):10513-8 PMID: 18663219
  64. Mechanisms of cellular communication through intercellular protein transfer.
    J Cell Mol Med. 2011 Jul;15(7):1458-73 PMID: 20070437
  65. EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell lines.
    Ann Oncol. 2008 Jun;19(6):1053-9 PMID: 18304967
  66. Exosomes: extracellular organelles important in intercellular communication.
    J Proteomics. 2010 Sep 10;73(10):1907-20 PMID: 20601276
  67. Detection of microRNA expression in human peripheral blood microvesicles.
    PLoS One. 2008;3(11):e3694 PMID: 19002258
  68. Molecular characterisation of the tumour microenvironment in breast cancer.
    Eur J Cancer. 2008 Dec;44(18):2760-5 PMID: 19026532
  69. Secreted monocytic miR-150 enhances targeted endothelial cell migration.
    Mol Cell. 2010 Jul 9;39(1):133-44 PMID: 20603081
  70. microRNA-150 regulates mobilization and migration of bone marrow-derived mononuclear cells by targeting Cxcr4.
    PLoS One. 2011;6(10):e23114 PMID: 22039399
  71. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells.
    Nat Commun. 2011;2:282 PMID: 21505438
  72. Characterization of extracellular circulating microRNA.
    Nucleic Acids Res. 2011 Sep 1;39(16):7223-33 PMID: 21609964
Article Info
Journal
Pharmacology & therapeutics
Abbr.
Pharmacol Ther
ISSN
1879-016X
DOI
10.1016/j.pharmthera.2012.08.003
Published
2012-11-00
Epub
2012-00-08
Pages
169-74
Language
English
Region
England
NLM ID
7905840
PMCID
PMC3855335
Subset
IM
Grants
NCI NIH HHS · R01 CA135444 · United States
NCI NIH HHS · R01 CA164346 · United States
NCI NIH HHS · CA100632 · United States
External Links
PubMed source DOI: 10.1016/j.pharmthera.2012.08.003 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2