- About this Journal ·
- Abstracting and Indexing ·
- Advance Access ·
- Aims and Scope ·
- Annual Issues ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2012 (2012), Article ID 354605, 10 pages
Ultrastructural Evidence of Exosome Secretion by Progenitor Cells in Adult Mouse Myocardium and Adult Human Cardiospheres
1Molecular Cardiology Laboratory, Fondazione Cardiocentro Ticino, Via Tesserete, 6900 Lugano, Switzerland
2Ultrastructural Pathology, “Victor Babeş” National Institute of Pathology, 99-101 Spl. Independentei, 050096 Bucharest 5, Romania
3Department of Cardiology, Centre Hospitalier Universitaire Vaudois (CHUV), Avenue du Bugnon, 1011 Lausanne, Switzerland
Received 18 June 2012; Accepted 16 July 2012
Academic Editor: Ken-ichi Isobe
Copyright © 2012 Lucio Barile et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- D. Orlic, J. Kajstura, S. Chimenti et al., “Bone marrow cells regenerate infarcted myocardium,” Nature, vol. 410, no. 6829, pp. 701–705, 2001.
- L. B. Balsam, A. J. Wagers, J. L. Christensen, T. Kofidis, I. L. Weissmann, and R. C. Robbins, “Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium,” Nature, vol. 428, no. 6983, pp. 668–673, 2004.
- C. E. Murry, M. H. Soonpaa, H. Reinecke et al., “Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts,” Nature, vol. 428, no. 6983, pp. 664–668, 2004.
- C. Stamm, B. Westphal, H. D. Kleine et al., “Autologous bone-marrow stem-cell transplantation for myocardial regeneration,” The Lancet, vol. 361, no. 9351, pp. 45–46, 2003.
- K. C. Wollert, G. P. Meyer, J. Lotz et al., “Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial,” The Lancet, vol. 364, no. 9429, pp. 141–148, 2004.
- V. Schächinger, S. Erbs, A. Elsässer et al., “Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction,” The New England Journal of Medicine, vol. 355, no. 12, pp. 1210–1221, 2006.
- B. Assmus, J. Honold, V. Schächinger et al., “Transcoronary transplantation of progenitor cells after myocardial infarction,” The New England Journal of Medicine, vol. 355, no. 12, pp. 1222–1232, 2006.
- S. Janssens, C. Dubois, J. Bogaert et al., “Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial,” The Lancet, vol. 367, no. 9505, pp. 113–121, 2006.
- K. Lunde, S. Solheim, S. Aakhus et al., “Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction,” The New England Journal of Medicine, vol. 355, no. 12, pp. 1199–1209, 2006.
- E. Forte, I. Chimenti, L. Barile et al., “Cardiac cell therapy: the next (re)generation,” Stem Cell Reviews and Reports, vol. 7, pp. 1018–1030, 2011.
- E. Chavakis, M. Koyanagi, and S. Dimmeler, “Enhancing the outcome of cell therapy for cardiac repair: progress from bench to bedside and back,” Circulation, vol. 121, no. 2, pp. 325–335, 2010.
- A. Abdel-Latif, R. Bolli, I. M. Tleyjeh et al., “Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis,” Archives of Internal Medicine, vol. 167, no. 10, pp. 989–997, 2007.
- K. C. Wollert and H. Drexler, “Cell therapy for the treatment of coronary heart disease: a critical appraisal,” Nature Reviews Cardiology, vol. 7, no. 4, pp. 204–215, 2010.
- D. M. Leistner, U. Fischer-Rasokat, J. Honold et al., “Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI): final 5-year results suggest long-term safety and efficacy,” Clinical Research in Cardiology, vol. 100, no. 10, pp. 925–934, 2011.
- S. Dimmeler and A. Leri, “Aging and disease as modifiers of efficacy of cell therapy,” Circulation Research, vol. 102, no. 11, pp. 1319–1330, 2008.
- H. Ebelt, M. Jungblut, Y. Zhang et al., “Cellular cardiomyoplasty: improvement of left ventricular function correlates with the release of cardioactive cytokines,” Stem Cells, vol. 25, no. 1, pp. 236–244, 2007.
- K. R. Vrijsena, S. A. J. Chamuleaua, W. A. Noorta, P. A. Doevendansa, and J. P. G. Sluijtera, “Stem cell therapy for end-stage heart failure: indispensable role for the cell?” Current Opinion in Organ Transplantation, vol. 14, no. 5, pp. 560–565, 2009.
- M. Gnecchi, Z. Zhang, A. Ni, and V. J. Dzau, “Paracrine mechanisms in adult stem cell signaling and therapy,” Circulation Research, vol. 103, no. 11, pp. 1204–1219, 2008.
- S. Ausoni and S. Sartore, “The cardiovascular unit as a dynamic player in disease and regeneration,” Trends in Molecular Medicine, vol. 15, no. 12, pp. 543–552, 2009.
- K. Urbanek, D. Cesselli, M. Rota et al., “Stem cell niches in the adult mouse heart,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 24, pp. 9226–9231, 2006.
- A. P. Beltrami, L. Barlucchi, D. Torella et al., “Adult cardiac stem cells are multipotent and support myocardial regeneration,” Cell, vol. 114, no. 6, pp. 763–776, 2003.
- H. Oh, S. B. Bradfute, T. D. Gallardo et al., “Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 21, pp. 12313–12318, 2003.
- H. C. Ott, T. S. Matthiesen, J. Brechtken et al., “The adult human heart as a source for stem cells: repair strategies with embryonic-like progenitor cells,” Nature Clinical Practice Cardiovascular Medicine, vol. 4, supplement 1, pp. S27–S39, 2007.
- C. Bearzi, M. Rota, T. Hosoda et al., “Human cardiac stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 35, pp. 14068–14073, 2007.
- R. R. Smith, L. Barile, H. C. Cho et al., “Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens,” Circulation, vol. 115, no. 7, pp. 896–908, 2007.
- A. Linke, P. Müller, D. Nurzynska et al., “Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 25, pp. 8966–8971, 2005.
- A. M. Smits, P. van Vliet, C. H. Metz et al., “Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology,” Nature Protocols, vol. 4, no. 2, pp. 232–243, 2009.
- L. Barile, I. Chimenti, R. Gaetani et al., “Cardiac stem cells: isolation, expansion and experimental use for myocardial regeneration,” Nature Clinical Practice Cardiovascular Medicine, vol. 4, supplement 1, pp. S9–S14, 2007.
- L. Barile, E. Messina, A. Giacomello, and E. Marbán, “Endogenous cardiac stem cells,” Progress in Cardiovascular Diseases, vol. 50, no. 1, pp. 31–48, 2007.
- G. M. Ellison, V. Galuppo, C. Vicinanza et al., “Cardiac stem and progenitor cell identification: different markers for the same cell?” Frontiers in Bioscience, vol. 2, pp. 641–652, 2010.
- L. Barile, F. Cerisoli, G. Frati et al., “Bone marrow-derived cells can acquire cardiac stem cells properties in damaged heart,” Journal of Cellular and Molecular Medicine, vol. 15, no. 1, pp. 63–71, 2011.
- S. S. Fazel, L. Chen, D. Angoulvant et al., “Activation of c-kit is necessary for mobilization of reparative bone marrow progenitor cells in response to cardiac injury,” The FASEB Journal, vol. 22, no. 3, pp. 930–940, 2008.
- L. W. van Laake, L. Qian, P. Cheng et al., “Reporter-based isolation of induced pluripotent stem cell-and embryonic stem cell-derived cardiac progenitors reveals limited gene expression variance,” Circulation Research, vol. 107, no. 3, pp. 340–347, 2010.
- Y. Yoshida and S. Yamanaka, “IPS cells: a source of cardiac regeneration,” Journal of Molecular and Cellular Cardiology, vol. 50, no. 2, pp. 327–332, 2011.
- B. A. Reynolds and S. Weiss, “Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system,” Science, vol. 255, no. 5052, pp. 1707–1710, 1992.
- E. Pastrana, V. Silva-Vargas, and F. Doetsch, “Eyes wide open: a critical review of sphere-formation as an assay for stem cells,” Cell Stem Cell, vol. 8, no. 5, pp. 486–498, 2011.
- E. Messina, L. De Angelis, G. Frati et al., “Isolation and expansion of adult cardiac stem cells from human and murine heart,” Circulation Research, vol. 95, no. 9, pp. 911–921, 2004.
- T. S. Li, K. Cheng, S. T. Lee et al., “Cardiospheres recapitulate a niche-like microenvironment rich in stemness and cell-matrix interactions, rationalizing their enhanced functional potency for myocardial repair,” Stem Cells, vol. 28, no. 11, pp. 2088–2098, 2010.
- D. R. Davis, Y. Zhang, R. R. Smith et al., “Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue,” PLoS ONE, vol. 4, no. 9, Article ID e7195, 2009.
- D. C. Andersen, P. Andersen, M. Schneider, H. B. Jensen, and S. P. Sheikh, “Murine “cardiospheres” are not a source of stem cells with cardiomyogenic potential,” Stem Cells, vol. 27, no. 7, pp. 1571–1581, 2009.
- I. Chimenti, R. R. Smith, T. S. Li et al., “Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice,” Circulation Research, vol. 106, no. 5, pp. 971–980, 2010.
- R. Bolli, A. R. Chugh, D. D'Amario, et al., “Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial,” The Lancet, vol. 378, no. 9806, pp. 1847–1857, 2011.
- R. R. Makkar, R. R. Smith, K. Cheng, et al., “Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial,” The Lancet, vol. 379, no. 9819, pp. 895–904, 2012.
- X. L. Tang, G. Rokosh, S. K. Sanganalmath et al., “Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction,” Circulation, vol. 121, no. 2, pp. 293–305, 2010.
- A. M. Smits, L. W. Van Laake, K. Den Ouden et al., “Human cardiomyocyte progenitor cell transplantation preserves long-term function of the infarcted mouse myocardium,” Cardiovascular Research, vol. 83, no. 3, pp. 527–535, 2009.
- E. Kizana, E. Cingolani, and E. Marbán, “Non-cell-autonomous effects of vector-expressed regulatory RNAs in mammalian heart cells,” Gene Therapy, vol. 16, no. 9, pp. 1163–1168, 2009.
- P. R. Crisostomo, A. M. Abarbanell, M. Wang, T. Lahm, Y. Wang, and D. R. Meldrum, “Embryonic stem cells attenuate myocardial dysfunction and inflammation after surgical global ischemia via paracrine actions,” American Journal of Physiology, vol. 295, no. 4, pp. H1726–H1735, 2008.
- M. Gnecchi, H. He, N. Noiseux et al., “Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement,” The FASEB Journal, vol. 20, no. 6, pp. 661–669, 2006.
- L. Timmers, S. K. Lim, F. Arslan et al., “Reduction of myocardial infarct size by human mesenchymal stem cell conditioned medium,” Stem Cell Research, vol. 1, no. 2, pp. 129–137, 2008.
- F. Bönner, N. Borg, S. Burghoff, and J. Schrader, “Resident cardiac immune cells and expression of the ectonucleotidase enzymes CD39 and CD73 after ischemic injury,” PLoS One, vol. 7, Article ID e34730, 2012.
- S. F. Mause and C. Weber, “Microparticles: protagonists of a novel communication network for intercellular information exchange,” Circulation Research, vol. 107, no. 9, pp. 1047–1057, 2010.
- C. Théry, “Exosomes: secreted vesicles and intercellular communications,” F1000 Biology Reports, vol. 3, no. 1, article 15, 2011.
- C. Théry, S. Amigorena, G. Raposo, and A. Clayton, “Isolation and characterization of exosomes from cell culture supernatants and biological fluids,” Current Protocols in Cell Biology, vol. 3, article 22, 2006.
- S. Mathivanan, H. Ji, and R. J. Simpson, “Exosomes: extracellular organelles important in intercellular communication,” Journal of Proteomics, vol. 73, no. 10, pp. 1907–1920, 2010.
- P. J. Quesenberry and J. M. Aliotta, “Cellular phenotype switching and microvesicles,” Advanced Drug Delivery Reviews, vol. 62, no. 12, pp. 1141–1148, 2010.
- S. Mathivanan and R. J. Simpson, “ExoCarta: a compendium of exosomal proteins and RNA,” Proteomics, vol. 9, no. 21, pp. 4997–5000, 2009.
- M. Ostrowski, N. B. Carmo, S. Krumeich et al., “Rab27a and Rab27b control different steps of the exosome secretion pathway,” Nature cell biology, vol. 12, no. 1, pp. 19–3013, 2010.
- H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J. J. Lee, and J. O. Lötvall, “Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells,” Nature Cell Biology, vol. 9, no. 6, pp. 654–659, 2007.
- J. Ratajczak, K. Miekus, M. Kucia et al., “Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery,” Leukemia, vol. 20, no. 5, pp. 847–856, 2006.
- K. Ohshima, K. Inoue, A. Fujiwara et al., “Let-7 microRNA family Is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line,” PLoS ONE, vol. 5, no. 10, Article ID e13247, 2010.
- A. Montecalvo, A. T. Larregina, W. J. Shufesky, et al., “Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes,” Blood, vol. 119, no. 3, pp. 756–766, 2012.
- S. Sahoo, E. Klychko, T. Thorne, et al., “Exosomes from human CD34+ stem cells mediate their proangiogenic paracrine activity,” Circulation Research, vol. 109, pp. 724–728, 2011.
- K. R. Vrijsen, J. P. G. Sluijter, M. W. L. Schuchardt et al., “Cardiomyocyte progenitor cell-derived exosomes stimulate migration of endothelial cells,” Journal of Cellular and Molecular Medicine, vol. 14, no. 5, pp. 1064–1070, 2010.
- R. C. Lai, T. S. Chen, and S. K. Lim, “Mesenchymal stem cell exosome: a novel stem cell-based therapy for cardiovascular disease,” Regenerative Medicine, vol. 6, no. 4, pp. 481–492, 2011.
- R. C. Lai, F. Arslan, M. M. Lee et al., “Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury,” Stem Cell Research, vol. 4, no. 3, pp. 214–222, 2010.
- E. Emmanouilidou, K. Melachroinou, T. Roumeliotis et al., “Cell-produced α-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival,” Journal of Neuroscience, vol. 30, no. 20, pp. 6838–6851, 2010.
- P. G. Sreekumar, R. Kannan, M. Kitamura et al., “αB crystallin is apically secreted within exosomes by polarized human retinal pigment epithelium and provides neuroprotection to adjacent cells,” PLoS ONE, vol. 5, no. 10, Article ID e12578, 2010.
- M. Gherghiceanu and L. M. Popescu, “Cardiac telocytes—their junctions and functional implications,” Cell Tissue Research, vol. 348, no. 2, pp. 265–279, 2012.
- L. M. Popescu and M. S. Faussone-Pellegrini, “TELOCYTES—a case of serendipity: the winding way from Interstitial Cells of Cajal (ICC), via Interstitial Cajal-Like Cells (ICLC) to TELOCYTES,” Journal of Cellular and Molecular Medicine, vol. 14, no. 4, pp. 729–740, 2010.
- M. Gherghiceanu and L. M. Popescu, “Cardiomyocyte precursors and telocytes in epicardial stem cell niche: electron microscope images,” Journal of Cellular and Molecular Medicine, vol. 14, no. 4, pp. 871–877, 2010.
- C. G. Manole, V. Cismaşiu, M. Gherghiceanu, and L. M. Popescu, “Experimental acute myocardial infarction: telocytes involvement in neo-angiogenesis,” Journal of Cellular and Molecular Medicine, vol. 15, no. 11, pp. 2284–2296, 2011.
- H. Yagi, A. Soto-Gutierrez, B. Parekkadan et al., “Mesenchymal stem cells: mechanisms of immunomodulation and homing,” Cell Transplantation, vol. 19, no. 6-7, pp. 667–679, 2010.
- L. Zitvogel, A. Regnault, A. Lozier et al., “Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes,” Nature Medicine, vol. 4, no. 5, pp. 594–600, 1998.
- B. Escudier, T. Dorval, N. Chaput et al., “Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase 1 clinical trial,” Journal of Translational Medicine, vol. 3, article 10, 2005.
- M. A. Morse, J. Garst, T. Osada et al., “A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer,” Journal of Translational Medicine, vol. 3, article 9, 2005.
- S. Dai, D. Wei, Z. Wu et al., “Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer,” Molecular Therapy, vol. 16, no. 4, pp. 782–790, 2008.
- K. Malliaras, T. S. Li, D. Luthringer, et al., “Safety and efficacy of allogeneic cell therapy in infarcted rats transplanted with mismatched cardiosphere-derived cells,” Circulation, vol. 125, pp. 100–112, 2012.
- N. Chaput and C. Théry, “Exosomes: immune properties and potential clinical implementations,” Seminars in Immunopathology, vol. 33, no. 5, pp. 419–440, 2011.