Top

Published in:

Open Access 01-08-2013 | Review

Extracellular vesicles as an emerging mechanism of cell-to-cell communication

Authors: Ciro Tetta, Ezio Ghigo, Lorenzo Silengo, Maria Chiara Deregibus, Giovanni Camussi

Published in: Endocrine | Issue 1/2013

Abstract

The concept that extracellular vesicles may act as paracrine/endocrine effectors is based on the evidence that they are able to transport bioactive molecules between cells, either within a defined microenvironment or remotely, by entering the biologic fluids. Extracellular vesicles, including exosomes and microvesicles, may deliver lipids and various functional transcripts, released from the cell of origin, to target cells. Since extracellular vesicles contain defined patterns of mRNA, microRNA, long non-coding RNA, and occasionally genomic DNA, they may transfer genetic information which induces transient or persistent phenotypic changes in recipient cells. In this review, we will discuss potential physiologic and pathological implications of extracellular vesicles, as well as the diagnostic and therapeutic opportunities that they may provide.

G. Camussi, M.C. Deregibus, S. Bruno, V. Cantaluppi, L. Biancone, Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 78, 838–848 (2010)PubMedCrossRef

A. Michael, S.D. Bajracharya, P.S. Yuen, H. Zhou, R.A. Star, G.G. Illei, I. Alevizos, Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 16, 34–38 (2010)PubMedCrossRef

A. Lakkaraju, E. Rodriguez-Boulan, Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol. 18, 199–209 (2008)PubMedCrossRef

N. Kosaka, H. Izumi, K. Sekine, T. Ochiya, microRNA as a new immune-regulatory agent in breast milk. Silence 1, 7–14 (2010)PubMedCrossRef

S. Keller, C. Rupp, A. Stoeck, S. Runz, M. Fogel, S. Lugert, H.D. Hager, M.S. Abdel-Bakky, P. Gutwein, P. Altevogt, CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int. 72, 1095–1102 (2007)PubMedCrossRef

T. Pisitkun, R.F. Shen, M.A. Knepper, Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. USA 101, 13368–13373 (2004)PubMedCrossRef

J. Nilsson, J. Skog, A. Nordstrand, V. Baranov, L. Mincheva-Nilsson, X.O. Breakefield, A. Widmark, Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. Br. J. Cancer 100, 1603–1607 (2009)PubMedCrossRef

J. Ratajczak, M. Wysoczynski, F. Hayek, A. Janowska-Wieczorek, M.Z. Ratajczak, Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487–1495 (2006)PubMedCrossRef

K. Schara, V. Jansa, V. Sustar, D. Dolinar, J.I. Pavlic, M. Lokar, V. Kralj-Iglic, P. Veranic, A. Iglic, Mechanisms for the formation of membranous nanostructures in cell-to-cell communication. Cell. Mol. Biol. Lett. 14, 636–656 (2009)PubMedCrossRef

10.

F. Bianco, C. Perrotta, L. Novellino, M. Francolini, L. Riganti, E. Menna, L. Saglietti, E.H. Schuchman, R. Furlan, E. Clementi, M. Matteoli, C. Verderio, Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J. 28, 1043–1054 (2009)PubMedCrossRef

11.

V. Muralidharan-Chari, J.W. Clancy, A. Sedgwick, C. D’Souza-Schorey, Microvesicles: mediators of extracellular communication during cancer progression. J. Cell Sci. 123, 1603–1611 (2010)PubMedCrossRef

12.

R.L. Williams, S. Urbé, The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355–368 (2007)PubMedCrossRef

13.

K. Trajkovic, C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brügger, M. Simons, Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244–1247 (2008)PubMedCrossRef

14.

G. van Niel, S. Charrin, S. Simoes, M. Romao, L. Rochin, P. Saftig, M.S. Marks, E. Rubinstein, G. Raposo, The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev. Cell 21, 708–721 (2011)PubMedCrossRef

15.

F.J. Verweij, M.A. van Eijndhoven, E.S. Hopmans, T. Vendrig, T. Wurdinger, E. Cahir-McFarland, E. Kieff, D. Geerts, R. van der Kant, J. Neefjes, J.M. Middeldorp, D.M. Pegtel, LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-κB activation. EMBO J. 30, 2115–2129 (2011)PubMedCrossRef

16.

Y. Fang, N. Wu, X. Gan, W. Yan, J.C. Morrell, S.J. Gould, Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol. 5, e158 (2007)PubMedCrossRef

17.

E. Cocucci, G. Racchetti, J. Meldolesi, Shedding microvesicles: artefacts no more. Trends Cell Biol. 19, 43–51 (2008)CrossRef

18.

B.J. Quah, V.P. Barlow, V. McPhun, K.I. Matthaei, M.D. Hulett, C.R. Parish, Bystander B cells rapidly acquire antigen receptors from activated B cells by membrane transfer. Proc. Natl. Acad. Sci. USA 105, 4259–4264 (2008)PubMedCrossRef

19.

J.W. Kim, E. Wieckowski, D.D. Taylor, T.E. Reichert, S. Watkins, T.L. Whiteside, Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin. Cancer Res. 11, 1010–1020 (2005)PubMed

20.

J. Yu, L. May, C. Milsom, G.M. Anderson, J.I. Weitz, J.P. Luyendyk, G. Broze, N. Mackman, J. Rak, Contribution of host-derived tissue factor to tumor neovascularization. Arterioscler. Thromb. Vasc. Biol. 28, 1975–1981 (2008)PubMedCrossRef

21.

K. Al-Nedawi, B. Meehan, R.S. Kerbel, A.C. Allison, J. Rak, Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc. Natl. Acad. Sci. USA 106, 3794–3799 (2009)PubMedCrossRef

22.

A. Sarkar, S. Mitra, S. Mehta, R. Raices, M.D. Wewers, Monocyte derived microvesicles deliver a cell death message via encapsulated caspase-1. PLoS ONE 4, e7140 (2009)PubMedCrossRef

23.

H. Sheldon, E. Heikamp, H. Turley, R. Dragovic, P. Thomas, C.E. Oon, R. Leek, M. Edelmann, B. Kessler, R.C. Sainson, I. Sargent, J.L. Li, A.L. Harris, New mechanism for notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood 116, 2385–2394 (2010)PubMedCrossRef

24.

C. Frühbeis, D. Fröhlich, E.M. Krämer-Albers, Emerging roles of exosomes in neuron-glia communication. Front. Physiol. 3, 119 (2012)PubMedCrossRef

25.

L.J. Vella, D.L. Greenwood, R. Cappai, J.P. Scheerlinck, A.F. Hill, Enrichment of prion protein in exosomes derived from ovine cerebral spinal fluid. Vet. Immunol. Immunopathol. 124, 385–393 (2008)PubMedCrossRef

26.

K. Al-Nedawi, B. Meehan, J. Micallef, V. Lhotak, L. May, A. Guha, J. Rak, Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 10, 619–624 (2008)PubMedCrossRef

27.

A. Schneider, M. Simons, Exosomes: vesicular carriers for intercellular communication in neurodegenerative disorders. Cell Tissue Res. (2012) DOI: 10.1007/s00441-012-1428-2

28.

B. Fevrier, D. Vilette, F. Archer, D. Loew, W. Faigle, M. Vidal, H. Laude, G. Raposo, Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. USA 101, 9683–9688 (2004)PubMedCrossRef

29.

X. Chen, H. Liang, J. Zhang, K. Zen, C.Y. Zhang, Secreted microRNAs: a new form of intercellular communication. Trends Cell Biol. 22, 125–132 (2012)PubMedCrossRef

30.

J. Krol, I. Loedige, W. Filipowicz, The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597–610 (2010)PubMed

31.

M.C. Deregibus, V. Cantaluppi, R. Calogero, M. Lo Iacono, C. Tetta, L. Biancone, S. Bruno, B. Bussolati, G. Camussi, Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110, 2440–2448 (2007)PubMedCrossRef

32.

J.M. Aliotta, M. Pereira, K.W. Johnson, N. de Paz, M.S. Dooner, N. Puente, C. Ayala, K. Brilliant, D. Berz, D. Lee, B. Ramratnam, P.N. McMillan, D.C. Hixson, D. Josic, P.J. Quesenberry, Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription. Exp. Hematol. 38, 233–245 (2010)PubMedCrossRef

33.

S. Bruno, C. Grange, M.C. Deregibus, R.A. Calogero, S. Saviozzi, F. Collino, L. Morando, A. Busca, M. Falda, B. Bussolati, C. Tetta, G. Camussi, Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J. Am. Soc. Nephrol. 20, 1053–1067 (2009)PubMedCrossRef

34.

H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J.J. Lee, J.O. Lötvall, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654–659 (2007)PubMedCrossRef

35.

A. Yuan, E.L. Farber, A.L. Rapoport, D. Tejada, R. Deniskin, N.B. Akhmedov, D.B. Farber, Transfer of microRNAs by embryonic stem cell microvesicles. PLoS ONE 4, e4722 (2009)PubMedCrossRef

36.

F. Collino, M.C. Deregibus, S. Bruno, L. Sterpone, G. Aghemo, L. Viltono, C. Tetta, G. Camussi, Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS ONE 5, e11803 (2010)PubMedCrossRef

37.

V. Fonsato, F. Collino, M.B. Herrera, C. Cavallari, M.C. Deregibus, B. Cisterna, S. Bruno, R. Romagnoli, M. Salizzoni, C. Tetta, G. Camussi, Human liver stem cell-derived microvesicles inhibit hepatoma growth in SCID mice by delivering antitumor microRNAs. Stem Cells 30, 1985–1998 (2012)PubMedCrossRef

38.

A. Waldenström, N. Gennebäck, U. Hellman, G. Ronquist, Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS ONE 7, e34653 (2012)PubMedCrossRef

39.

K.G. Ronquist, G. Ronquist, L. Carlsson, A. Larsson, Human prostasomes contain chromosomal DNA. Prostate 69, 737–743 (2009)PubMedCrossRef

40.

M. Guescini, S. Genedani, V. Stocchi, L.F. Agnati, Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J. Neural Transm. 117, 1–4 (2010)PubMedCrossRef

41.

R.M. O’Connell, D.S. Rao, A.A. Chaudhuri, D. Baltimore, Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111–122 (2010)PubMedCrossRef

42.

G. Raposo, H.W. Nijman, W. Stoorvogel, R. Liejendekker, C.V. Harding, C.J. Melief, H.J. Geuze, B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183, 1161–1172 (1996)PubMedCrossRef

43.

L. Zitvogel, A. Regnault, A. Lozier, J. Wolfers, C. Flament, D. Tenza, P. Ricciardi-Castagnoli, G. Raposo, S. Amigorena, Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med. 4, 594–600 (1998)PubMedCrossRef

44.

E. Segura, C. Nicco, B. Lombard, P. Veron, G. Raposo, F. Batteux, S. Amigorena, C. Thery, ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 106, 216–223 (2005)PubMedCrossRef

45.

M. Baj-Krzyworzeka, J. Baran, K. Weglarczyk, R. Szatanek, A. Szaflarska, M. Siedlar, M. Zembala, Tumour-derived microvesicles (TMV) mimic the effect of tumour cells on monocyte subpopulations. Anticancer Res. 30, 3515–3519 (2010)PubMed

46.

A. Bobrie, M. Colombo, G. Raposo, C. Théry, Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 12, 1659–1668 (2011)PubMedCrossRef

47.

M. Mittelbrunn, C. Gutierrez-Vazquez, C. Villarroya-Beltri, S. Gonzalez, F. Sanchez-Cabo, M.A. Gonzalez, A. Bernad, F. Sanchez-Madrid, Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat. Commun. 2, 282 (2011)PubMedCrossRef

48.

S.I. Buschow, E.N. Nolte-’t Hoen, G. van Niel, M.S. Pols, T. Ten Broeke, M. Lauwen, F. Ossendorp, C.J. Melief, G. Raposo, R. Wubbolts, M.H. Wauben, W. Stoorvogel, MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic 10, 1528–1542 (2009)PubMedCrossRef

49.

D. Castellana, C. Kunzelmann, J.M. Freyssinet, Pathophysiologic significance of procoagulant microvesicles in cancer disease and progression. Hamostaseologie 29, 1–57 (2009)

50.

G. Andreola, L. Rivoltini, C. Castelli, V. Huber, P. Perego, P. Deho, P. Squarcina, P. Accornero, F. Lozupone, L. Lugini, A. Stringaro, A. Molinari, G. Arancia, M. Gentile, G. Parmiani, S. Fais, Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J. Exp. Med. 195, 1303–1316 (2002)PubMedCrossRef

51.

D. Castellana, F. Zobairi, M.C. Martinez, M.A. Panaro, V. Mitolo, J.M. Freyssinet, C. Kunzelmann, Membrane microvesicles as actors in the establishment of a favorable prostatic tumoral niche: a role for activated fibroblasts and CX3CL1-CX3CR1 axis. Cancer Res. 69, 69785–69793 (2009)CrossRef

52.

M. Baj-Krzyworzeka, K. Weglarczyk, B. Mytar, R. Szatanek, J. Baran, M. Zembala, Tumour-derived microvesicles contain interleukin-8 and modulate production of chemokines by human monocytes. Anticancer Res. 31, 1329–1335 (2011)PubMed

53.

M.A. Antonyak, B. Li, L.K. Boroughs, J.L. Johnson, J.E. Druso, K.L. Bryant, D.A. Holowka, R.A. Cerione, Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc. Natl. Acad. Sci. USA 108, 4852–4857 (2011)PubMedCrossRef

54.

M. Baj-Krzyworzeka, R. Szatanek, K. Weglarczyk, J. Baran, B. Urbanowicz, P. Brański, M.Z. Ratajczak, M. Zembala, Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol. Immunother. 55, 808–818 (2006)PubMedCrossRef

55.

J. Skog, T. Würdinger, S. van Rijn, D.H. Meijer, L. Gainche, M. Sena-Esteves, W.T. Jr Curry, B.S. Carter, A.M. Krichevsky, X.O. Breakefield, Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470–1476 (2008)PubMedCrossRef

56.

B.S. Hong, J.H. Cho, H. Kim, E.J. Choi, S. Rho, J. Kim, J.H. Kim, D.S. Choi, Y.K. Kim, D. Hwang, Y.S. Gho, Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genomics 10, 556–568 (2009)PubMedCrossRef

57.

M. Del Tatto, T. Ng, J.M. Aliotta, G.A. Colvin, M.S. Dooner, D. Berz, G.J. Dooner, E.F. Papa, D.C. Hixson, B. Ramratnam, B.I. Aswad, E.H. Sears, J. Reagan, P.J. Quesenberry, Marrow cell genetic phenotype change induced by human lung cancer cells. Exp. Hematol. 39, 1072–1080 (2011)PubMedCrossRef

58.

J.F. Renzulli II, M. Del Tatto, G. Dooner, J. Aliotta, L. Goldstein, M. Dooner, G. Colvin, D. Chatterjee, P. Quesenberry, Microvesicle induction of prostate specific gene expression in normal human bone marrow cells. J. Urol. 184, 2165–2171 (2010)PubMedCrossRef

59.

C. Grange, M. Tapparo, F. Collino, L. Vitillo, C. Damasco, M.C. Deregibus, C. Tetta, B. Bussolati, G. Camussi, Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 71, 5346–5356 (2011)PubMedCrossRef

60.

J. Ratajczak, K. Miekus, M. Kucia, J. Zhang, R. Reca, P. Dvorak, M.Z. Ratajczak, Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20, 847–856 (2006)PubMedCrossRef

61.

V. Cantaluppi, S. Gatti, D. Medica, F. Figliolini, S. Bruno, M.C. Deregibus, A. Sordi, L. Biancone, C. Tetta, G. Camussi, Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 82, 412–427 (2012)PubMedCrossRef

62.

P.J. Quesenberry, M.S. Dooner, J.M. Aliotta, Stem cell plasticity revisited: the continuum marrow model and phenotypic changes mediated by microvesicles. Exp. Hematol. 38, 581–592 (2010)PubMedCrossRef

63.

G. Müller, Microvesicles/exosomes as potential novel biomarkers of metabolic diseases. Diabetes Metab. Syndr. Obes. 5, 247–282 (2012)PubMedCrossRef

64.

C. Cipolletta, K.E. Ryan, E.V. Hanna, E.R. Trimble, Activation of peripheral blood CD14+monocytes occurs in diabetes. Diabetes 54, 2779–2786 (2005)PubMedCrossRef

65.

F. Sabatier, P. Darmon, B. Hugel, V. Combes, M. Sanmarco, J.G. Velut, D. Arnoux, P. Charpiot, J.M. Freyssinet, C. Oliver, J. Sampol, F. Dignat-George, Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes 51, 2840–2845 (2002)PubMedCrossRef

66.

K.T. Tan, M.H. Tayebjee, H.S. Lim, G.Y. Lip, Clinically apparent atherosclerotic disease in diabetes is associated with an increase in platelet microparticle levels. Diabet. Med. 22, 1657–1662 (2005)PubMedCrossRef

67.

H. Koga, S. Sugiyama, K. Kugiyama, H. Fukushima, K. Watanabe, T. Sakamoto, M. Yoshimura, H. Jinnouchi, H. Ogawa, Elevated levels of remnant lipoproteins are associated with plasma platelet microparticles in patients with type-2 diabetes mellitus without obstructive coronary artery disease. Eur. Heart J. 27, 817–823 (2006)PubMedCrossRef

68.

A.L. Sun, J.T. Deng, G.J. Guan, S.H. Chen, Y.T. Liu, J. Cheng, Z.W. Li, X.H. Zhuang, F.D. Sun, H.P. Deng, Dipeptidyl peptidase-IV is a potential molecular biomarker in diabetic kidney disease. Diab. Vasc. Dis. Res. 9, 301–308 (2012)PubMedCrossRef

69.

G. Müller, S. Wied, E.A. Dearey, G. Biemer-Daub, Glycosylphosphatidylinositol-anchored proteins coordinate lipolysis inhibition between large and small adipocytes. Metabolism 60, 1021–1037 (2011)PubMedCrossRef

70.

F.F. van Doormaal, A. Kleinjan, M. Di Nisio, H.R. Büller, R. Nieuwland, Cell-derived microvesicles and cancer. Neth. J. Med. 67, 266–273 (2009)PubMed

71.

M. Logozzi, A. De Milito, L. Lugini, M. Borghi, L. Calabrò, M. Spada, M. Perdicchio, M.L. Marino, C. Federici, E. Iessi, D. Brambilla, G. Venturi, F. Lozupone, M. Santinami, V. Huber, M. Maio, L. Rivoltini, S. Fais, High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS ONE 4, e5219 (2009)PubMedCrossRef

72.

J. Baran, M. Baj-Krzyworzeka, K. Weglarczyk, R. Szatanek, M. Zembala, J. Barbasz, A. Czupryna, A. Szczepanik, M. Zembala, Circulating tumour-derived microvesicles in plasma of gastric cancer patients. Cancer Immunol. Immunother. 59, 841–850 (2010)PubMedCrossRef

73.

A.M. Friel, C. Corcoran, J. Crown, L. O’Driscoll, Relevance of circulating tumor cells, extracellular nucleic acids, and exosomes in breast cancer. Breast Cancer Res. Treat. 123, 613–625 (2010)PubMedCrossRef

74.

N. Kosaka, H. Iguchi, T. Ochiya, Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 101, 2087–2092 (2010)PubMedCrossRef

75.

D.D. Taylor, C. Gercel-Taylor, MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110, 13–21 (2008)PubMedCrossRef

76.

G. Rabinowits, C. Gerçel-Taylor, J.M. Day, D.D. Taylor, G.H. Kloecker, Exosomal microRNA: a diagnostic marker for lung cancer. Clin. Lung Cancer 10, 42–46 (2009)PubMedCrossRef

77.

A.V. Vlassov, S. Magdaleno, R. Setterquist, R. Conrad, Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta 1820, 940–948 (2012)PubMedCrossRef

78.

L. Biancone, S. Bruno, M.C. Deregibus, C. Tetta, G. Camussi, Therapeutic potential of mesenchymal stem cell-derived microvesicles. Nephrol. Dial. Transplant. 27, 3037–3042 (2012)PubMedCrossRef

79.

S. Bruno, C. Grange, F. Collino, M.C. Deregibus, V. Cantaluppi, L. Biancone, C. Tetta, G. Camussi, Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS ONE 7, e33115 (2012)PubMedCrossRef

80.

A. Ranghino, V. Cantaluppi, C. Grange, L. Vitillo, F. Fop, L. Biancone, M.C. Deregibus, C. Tetta, G.P. Segoloni, G. Camussi, Endothelial progenitor cell-derived microvesicles improve neovascularization in a murine model of hindlimb ischemia. Int. J. Immunopathol. Pharmacol. 25, 75–85 (2012)PubMed

81.

R.C. Lai, T.S. Chen, S.K. Lim, Mesenchymal stem cell exosome: a novel stem cell-based therapy for cardiovascular disease. Regen. Med. 6, 481–492 (2011)PubMedCrossRef

82.

M.B. Herrera, V. Fonsato, S. Gatti, M.C. Deregibus, A. Sordi, D. Cantarella, R. Calogero, B. Bussolati, C. Tetta, G. Camussi, Human liver stem cell-derived microvesicles accelerate hepatic regeneration in hepatectomized rats. J. Cell Mol. Med. 14, 1605–1618 (2010)PubMedCrossRef

Title: Extracellular vesicles as an emerging mechanism of cell-to-cell communication
Authors: Ciro Tetta
Ezio Ghigo
Lorenzo Silengo
Maria Chiara Deregibus
Giovanni Camussi
Publication date: 01-08-2013
Publisher: Springer US
Published in: Endocrine / Issue 1/2013
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI: https://doi.org/10.1007/s12020-012-9839-0

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2013

BRAF V600E associates with cytoplasmatic localization of p27kip1 and higher cytokeratin 19 expression in papillary thyroid carcinoma

The relationship between physical activity, restless legs syndrome, and health-related quality of life in type 2 diabetes

Risk factors for ulceration and amputation in diabetic foot: study in a cohort of 496 patients

Investigational anti-hyperglycemic agents: the future of type 2 diabetes therapy?

Erratum to: The aldosterone to renin ratio in the evaluation of patients with incidentally detected adrenal masses

Prolactin and sex steroids levels in congenital lifetime isolated GH deficiency

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials