Experimental Hematology
Volume 38, Issue 3 , Pages 233-245 , March 2010

Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription

  • Jason M. Aliotta

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA
    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Pulmonary, Sleep and Critical Care Medicine, Providence, RI., USA
    • Corresponding Author InformationOffprint requests to: Jason M. Aliotta, M.D., Divisions of Hematology/Oncology and Pulmonary, Sleep and Critical Care Medicine, Rhode Island Hospital, 7th Floor APC Building, 593 Eddy Street, Providence, RI 02903
    • ,
  • Mandy Pereira

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA
    • ,
  • Kevin W. Johnson

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA
    • ,
  • Nicole de Paz

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA
    • ,
  • Mark S. Dooner

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA
    • ,
  • Napoleon Puente

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Pulmonary, Sleep and Critical Care Medicine, Providence, RI., USA
    • ,
  • Carol Ayala

      Affiliations

    • Rhode Island Hospital, Division of Core Research Laboratories, (Transmission Electron Microscopy Facility), Providence, RI., USA
    • ,
  • Kate Brilliant

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA
    • ,
  • David Berz

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA
    • ,
  • David Lee

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Pulmonary, Sleep and Critical Care Medicine, Providence, RI., USA
    • ,
  • Bharat Ramratnam

      Affiliations

    • Laboratory of Retrovirology, Division of Infectious Diseases, Department of Medicine, The Warren Alpert Medical School of Brown University, Providence, RI., USA
    • ,
  • Paul N. McMillan

      Affiliations

    • Rhode Island Hospital, Division of Core Research Laboratories, (Transmission Electron Microscopy Facility), Providence, RI., USA
    • ,
  • Douglas C. Hixson

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA
    • ,
  • Djuro Josic

      Affiliations

    • Rhode Island Hospital, Proteomics Core, COBRE CCRD, Providence, RI., USA
    • ,
  • Peter J. Quesenberry

      Affiliations

    • Rhode Island Hospital, The Warren Alpert Medical School of Brown University, Division of Hematology and Oncology, Providence, RI., USA

Received 27 December 2009 ,Revised 4 January 2010 ,Accepted 5 January 2010.

References 

  1. Keller S, Sanderson MP, Stoeck A. Exosomes: from biogenesis and secretion to biological function. Immunol Lett. 2006;107:102–108
  2. Fader CM, Colombo MI. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ. 2009;16:70–78
  3. Morel O, Toti F, Hugel B, et al. Cellular microparticles: a disseminated storage pool of bioactive vascular effectors. Curr Opin Hematol. 2004;11:156–164
  4. Heijnen HF, Schiel AE, Fijnheer R, et al. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood. 1999;94:3791–3799
  5. Nomura S, Nakamura T, Cone J, et al. Cytometric analysis of high shear-induced platelet microparticles and effect of cytokines on microparticle generation. Cytometry. 2000;40:173–181
  6. Janowska-Wieczorek A, Majka M, Kijowski J, et al. Platelet-derived microparticles bind to hematopoietic stem/progenitor cells and enhance their engraftment. Blood. 2001;98:3143–3149
  7. Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nature Rev Immunol. 2009;9:581–593
  8. Baj-Krzyworzeka M, Szatanek R, Weglarczyk K, et al. Tumor-derived microvesicles carry several surface determinants and mRNA of tumor cells and transfer some of these determinants to monocytes. Cancer Immunol Imunother. 2006;55:808–818
  9. Rozmyslowicz T, Majka M, Kijowski J, et al. Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS. 2003;17:33–42
  10. Graves LE, Ariztia EV, Navari JR, et al. Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res. 2004;64:7045–7049
  11. Fackler OT, Peterlin BM. Endocytic entry of HIV-1. Curr Biol. 2000;10:1005–1008
  12. Fevrier B, Vilette D, Archer F. Cells release prions in association with exosomes. Proc Natl Acad Sci U S A. 2004;100:10592–10597
  13. Ratajczak J, Miekus K, Kucia M, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006;20:847–856
  14. Holmgren L, Szeles A, Rajnavolgyi R, et al. Horizontal transfer of DNA by the uptake of apoptotic bodies. Blood. 1999;93:3956–3963
  15. Hakelien AM, Landsverk HB, Rob JM, et al. Reprogramming fibroblasts to express T-cell functions using cell extracts. Nature Biotech. 2002;20:460–466
  16. Deregibus MC, Cantaluppi V, Calogero R, et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood. 2007;110:2440–2448
  17. Prokopi M, Pula G, Mayr U, et al. Proteomic analysis reveals presence of platelet microparticles in endothelial progenitor cell cultures. Blood. 2009;114:723–732
  18. Aliotta JM, Passero M, Meharg J, et al. Stem cells and pulmonary metamorphosis: new concepts in repair and regeneration. J Cell Physiol. 2005;204:725–741
  19. Krause DS. Engraftment of bone marrow-derived epithelial cells. Ann NY Acad Sci. 2005;1044:117–124
  20. Aliotta JM, Keaney P, Passero M, et al. Bone marrow production of lung cells: the impact of G-CSF, cardiotoxin, graded doses of irradiation, and subpopulation phenotype. Exp Hematol. 2006;34:230–241
  21. Aliotta JM, Sanchez-Guijo FM, Dooner GJ, et al. Alteration of marrow gene expression, protein production and engraftment into lung by lung-derived microvesicles. Stem Cells. 2007;9:2245–2256
  22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25:402–408
  23. Josic D, Brown MK, Huang F, et al. Proteomic characterization of inter-alpha inhibitor proteins from human plasma. Proteomics. 2006;6:2874–2885
  24. Lawson E, Clifton JG, Huang F, et al. Use of magnetic beads with immobilized monoclonal antibodies for isolation of highly pure plasma membranes. Electrophoresis. 2006;27:2747–2758
  25. Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosome: current perspectives. Proteomics. 2008;8:4083–4099
  26. Poliakov A, Spillman M, Dokland T, et al. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate. 2009;69:159–167
  27. Conde-Vancells JE, Rodriguez-Suarez N, Embade D, et al. Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J Proteome Res. 2008;7:5157–5166
  28. Liu Y, Shah SV, Xiang X, et al. COP9-Associated CSN5 regulates endosomal protein deubiquitination and sorting. Am J Pathol. 2009;174:1415–1425
  29. Looze C, Yui D, Leung L, et al. Proteomic profiling of human plasma exosmes identifies PPARgamma as an exosome-associated protein. Biochem Biophys Res Commun. 2009;378:433–438
  30. Gonzalez-Begne M, Lu B, Han X, et al. Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT). J Proteome Res. 2009;8:1304–1314
  31. Ji H, Erfani N, Tauro BJ, et al. Difference gel electrophoresis analysis of Ras-transformed fibroblast cell-derived exosomes. Electrophoresis. 2008;29:2660–2671
  32. Quesenberry PJ, Dooner G, Dooner M, et al. Developmental biology: Ignoratio elenchi: red herrings in stem cell research. Science. 2005;308:1121–1122
  33. Ong SE, Mann M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc. 2006;1:2650–2660
  34. Hunter MP, Ismail N, Zhang X, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One. 2008;3:e3694
  35. Skog J, Würdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–1476
  36. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008;110:1–2
  37. Chekanova JA, Gregory BD, Reverdatto SV, et al. Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell. 2007;131:1340–1353
  38. Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–659
  39. Tang X, Muniappan L, Tang G, et al. Identification of glucose-regulated miRNAs from pancreatic (beta) cells reveals a role for miR-30d in insulin transcription. RNA. 2009;15:287–293
  40. Wang G, Wang Y, Feng W, et al. Transcription factor and microRNA regulation in androgen-dependent and independent prostate cancer cells. BMC Genomics. 2008;9(Suppl):S22
  41. Korpal M, Lee ES, Hu G, et al. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem. 2008;283:14910–14914
  42. Li X, Zhang YZ. Conmputational detectyion of microRNAs targeting transcription factor genes in Arabidopsis thaliana. Comput Biol Chem. 2005;29:360–367
  43. Fujita Y, Kojima K, Hamada N, et al. Effects of miR-34a on cell growth and chemoresistance in prostate cancer PC3 cells. Biochem Biophys Res Commun. 2008;377:114–119
  44. Baroukh N, Ravier MA, Loder MK, et al. MicroRNA-124a regulates Foxa2 expression and intracellular signaling in pancreatic beta-cell lines. J Biol Chem. 2007;282:19575–19588
  45. Wysoczynski M, Ratajczak MZ. Lung cancer secreted microvesicles: underappreciated modulators of microenvironment in expanding tumors. Int J Cancer. 2009;125:1595–1603
  46. Lynch SF, Ludlam CA. Plasma microparticles and vascular disorders. Br J Haemtol. 2007;137:36–48
  47. Pihusch R, Höhnberg B, Salat C, et al. Platelet flow cytometric findings in patients undergoing conditioning therapy for allogeneic hematopoietic stem cell transplantation. Ann Hematol. 2002;81:454–461
  48. Ratajczak J, Wysoczynski M, Hayek F, et al. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia. 2006;20:1487–1495
  49. Aharon A, Brenner B. Microparticles, thrombosis and cancer. Best Pract Res Clin Haematol. 2009;22:61–69

PII: S0301-472X(10)00010-X

doi: 10.1016/j.exphem.2010.01.002

Experimental Hematology
Volume 38, Issue 3 , Pages 233-245 , March 2010

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