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Membrane-Derived Extracellular Vesicles from Endothelial Progenitor Cells Activate Angiogenesis

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Tumor Dormancy, Quiescence, and Senescence, Volume 2

Part of the book series: Tumor Dormancy and Cellular Quiescence and Senescence ((DOQU,volume 2))

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Abstract

The neoformation of blood vessels is a biological process involved in tissue homeostasis and repair as well as in pathologic conditions such as inflammatory diseases and cancer. Endothelial progenitor cells (EPCs) a cell population derived from the bone marrow and circulating in the blood stream, have been shown to take part to these processes. EPCs exert their effects mainly by the release of paracrine factors such as growth factors, cytokines and extracellular vesicles (EVs). EVs are small particles released by different types of activated cells by a membrane sorting process. Recent studies identified EVs as a new mechanism of cell-to-cell communication as they can mediate the exchange of receptors, proteins, bioactive lipids and nucleic acids between cells. EPC-derived EVs were shown to activate an angiogenic program in quiescent endothelial cells through an epigenetic reprogramming due to horizontal transfer of mRNA and microRNA. Whereas in the context of tumor neoangiogenesis this mechanism may be detrimental as it favors tumor vascularization and diffusion, in the context of regenerative medicine, EVs derived from EPCs can be exploited as potential therapeutic option to prevent ischemia-reperfusion injury.

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References

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

    Article  PubMed  Google Scholar 

  • Aliotta JM, Pereira M, Johnson KW, de Paz N, Dooner MS, Puente N, Ayala C, Brilliant K, Berz D, Lee D, Ramratnam B, McMillan PN, Hixson DC, Josic D, Quesenberry PJ (2010) 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

    Article  PubMed  CAS  Google Scholar 

  • Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967

    Article  PubMed  CAS  Google Scholar 

  • Baj-Krzyworzeka M, Szatanek R, Weglarczyk K, Baran J, Urbanowicz B, BraÅ„ski P, Ratajczak MZ, Zembala M (2006) 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

    Article  PubMed  CAS  Google Scholar 

  • Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, Skog J (2011) Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2:180

    Article  PubMed  Google Scholar 

  • Barry OP, Praticò D, Savani RC, FitzGerald GA (1998) Modulation of monocyte-endothelial cell interactions by platelet microparticles. J Clin Invest 102:136–144

    Article  PubMed  CAS  Google Scholar 

  • Biancone L, Cantaluppi V, Duò D, Deregibus MC, Torre C, Camussi G (2004) Role of L-selectin in the vascular homing of peripheral blood-derived endothelial progenitor cells. J Immunol 173:5268–5274

    PubMed  CAS  Google Scholar 

  • Bussolati B, Grange C, Camussi G (2011) Tumor exploits alternative strategies to achieve vascularization. FASEB J 25:2874–2882

    Article  PubMed  CAS  Google Scholar 

  • Cantaluppi V, Gatti S, Medica D, Figliolini F, Bruno S, Deregibus MC, Sordi A, Biancone L, Tetta C, Camussi G (2012a) 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

    Article  PubMed  CAS  Google Scholar 

  • Cantaluppi V, Biancone L, Figliolini F, Beltramo S, Medica D, Deregibus MC, Galimi F, Romagnoli R, Salizzoni M, Tetta C, Segoloni GP, Camussi G (2012b) Microvesicles derived from endothelial progenitor cells enhance neoangiogenesis of human pancreatic islets. Cell Transplant 21:1305–1320

    Article  PubMed  Google Scholar 

  • Castellana D, Toti F, Freyssinet JM (2010) Membrane microvesicles: macromessengers in cancer disease and progression. Thromb Res 125(Suppl 2):S84–S88

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • György B, Szabó TG, Pásztói M, Pál Z, Misják P, Aradi B, László V, Pállinger E, Pap E, Kittel A, Nagy G, Falus A, Buzás EI (2011) Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 68:2667–2688

    Article  PubMed  Google Scholar 

  • Kuwana T, Newmeyer DD (2003) Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15:691–699

    Article  PubMed  CAS  Google Scholar 

  • Lefer DJ, Lefer AM (1993) Nitric oxide homeostasis control as therapy for cardiovascular diseases. Cardiovasc Res 27:2282

    Article  PubMed  CAS  Google Scholar 

  • Li B, Cohen A, Hudson TE, Motlagh D, Amrani DL, Duffield JS (2010) Mobilized human hematopoietic stem/progenitor cells promote kidney repair after ischemia/reperfusion injury. Circulation 121:2211–2220

    Article  PubMed  Google Scholar 

  • Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, Wu Y, Hicklin D, Zhu Z, Hackett NR, Crystal RG, Moore MA, Hajjar KA, Manova K, Benezra R, Rafii S (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7:1194–1201

    Article  PubMed  CAS  Google Scholar 

  • Mathivanan S, Ji H, Simpson RJ (2010) Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73:1907–1920

    Article  PubMed  CAS  Google Scholar 

  • Millimaggi D, Mari M, D’Ascenzo S, Carosa E, Jannini EA, Zucker S, Carta G, Pavan A, Dolo V (2007) Tumor vesicle-associated CD147 modulates the angiogenic capability of endothelial cells. Neoplasia 9:349–357

    Article  PubMed  CAS  Google Scholar 

  • Nazarenko I, Rana S, Baumann A, McAlear J, Hellwig A, Trendelenburg M, Lochnit G, Preissner KT, Zöller M (2010) Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 70:1668–1678

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sarkar A, Mitra S, Mehta S, Raices R, Wewers MD (2009) Monocyte derived microvesicles deliver a cell death message via encapsulated caspase-1. PLoS One 4:e7140

    Article  PubMed  Google Scholar 

  • Schatteman GC, Dunnwald M, Jiao C (2007) Biology of bone marrow-derived endothelial cell precursors. Am J Physiol Heart Circ Physiol 292:H1–H18

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Simons M, Raposo G (2009) Exosomes–vesicular carriers for intercellular communication. Curr Opin Cell Biol 21:575–581

    Article  PubMed  CAS  Google Scholar 

  • Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10:1470–1476

    Article  PubMed  CAS  Google Scholar 

  • Théry C, Boussac M, Véron P, Ricciardi-Castagnoli P, Raposo G, Garin J, Amigorena S (2001) Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 166:7309–7318

    PubMed  Google Scholar 

  • Théry C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9:581–593

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659

    Article  PubMed  CAS  Google Scholar 

  • Wysoczynski M, Ratajczak MZ (2009) Lung cancer secreted microvesicles: underappreciated modulators of microenvironment in expanding tumors. Int J Cancer 125:1595–1603

    Article  PubMed  CAS  Google Scholar 

  • Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, Krasich R, Temm CJ, Prchal JT, Ingram DA (2007) Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109:1801–1809

    Article  PubMed  CAS  Google Scholar 

  • Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, Akhmedov NB, Farber DB (2009) Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 4:e4722

    Article  PubMed  Google Scholar 

  • Zampetaki A, Kirton JP, Xu Q (2008) Vascular repair by endothelial progenitor cells. Cardiovasc Res 78:413–421

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Giovanni Camussi .

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Cantaluppi, V., Figliolini, F., Deregibus, M.C., Camussi, G. (2014). Membrane-Derived Extracellular Vesicles from Endothelial Progenitor Cells Activate Angiogenesis. In: Hayat, M. (eds) Tumor Dormancy, Quiescence, and Senescence, Volume 2. Tumor Dormancy and Cellular Quiescence and Senescence, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7726-2_2

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