Exosome: A novel approach to stimulate bone regeneration through regulation of osteogenesis and angiogenesis

International Journal of Molecular Sciences

Volumn 17, Issue 5, 2016, Pages

  Qin, Yunhao ^a   Sun, Ruixin ^b   Wu, Chuanlong ^c   Wang, Lian ^d   Zhang, Changqing ^a  

^a SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^b FUDAN UNIVERSITY   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Bone regeneration; Exosome; Osteogenesis

Indexed keywords

ANGIOGENESIS; ATTENTION; BIOGENESIS; BONE GRAFT; BONE REGENERATION; CELL PROLIFERATION; DIFFERENTIATION; EXOSOME; HUMAN; IN VITRO STUDY; OSSIFICATION; SAFETY; TRANSCRIPTION REGULATION; TRAVEL; ANIMAL; BONE DEVELOPMENT; METABOLISM; PHYSIOLOGY;

ANIMALS; BONE REGENERATION; EXOSOMES; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOGENESIS;

EID: 84969277811     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17050712     Document Type: Review

References (81)

1. Van Griensven, M. Preclinical testing of drug delivery systems to bone. Adv. Drug Deliv. Rev. 2015, 94, 151-164.
2. Almubarak, S.; Nethercott, H.; Freeberg, M.; Beaudon, C.; Jha, A.; Jackson, W.; Marcucio, R.; Miclau, T.; Healy, K.; Bahney, C. Tissue engineering strategies for promoting vascularized bone regeneration. Bone 2015, 83, 197-209.
3. Chehade, M.J.; Bachorski, A. Development of the australian core competencies in musculoskeletal basic and clinical science project-Phase 1. Med. J. Aust. 2008, 189, 162-165.
4. Rodriguez-Merchan, E.C.; Forriol, F. Nonunion: General principles and experimental data. Clin. Orthop. Relat. Res. 2004, 419, 4-12.
5. Mankin, H.J.; Hornicek, F.J.; Raskin, K.A. Infection in massive bone allografts. Clin. Orthop. Relat. Res. 2005, 432, 210-216.
6. Schwartz, C.E.; Martha, J.F.; Kowalski, P.; Wang, D.A.; Bode, R.; Li, L.; Kim, D.H. Prospective evaluation of chronic pain associated with posterior autologous iliac crest bone graft harvest and its effect on postoperative outcome. Health Qual. Life Outcomes 2009, 7, 49.
7. Sorger, J.I.; Hornicek, F.J.; Zavatta, M.; Menzner, J.P.; Gebhardt, M.C.; Tomford, W.W.; Mankin, H.J. Allograft fractures revisited. Clin. Orthop. Relat. Res. 2001, 382, 66-74.
8. Dinopoulos, H.; Dimitriou, R.; Giannoudis, P.V. Bone graft substitutes: What are the options? Surgeon 2012, 10, 230-239.
9. Stafford, P.R.; Norris, B.L. Reamer-irrigator-aspirator bone graft and bi masquelet technique for segmental bone defect nonunions: A review of 25 cases. Injury 2010, 41, S72-S77.
10. Fleury, A.; Martinez, M.C.; Le Lay, S. Extracellular vesicles as therapeutic tools in cardiovascular diseases. Front. Immunol. 2014, 5, 370.
11. Mathivanan, S.; Ji, H.; Simpson, R.J. Exosomes: Extracellular organelles important in intercellular communication. J. Proteom. 2010, 73, 1907-1920.
12. Hoshino, A.; Costa-Silva, B.; Shen, T.L.; Rodrigues, G.; Hashimoto, A.; Tesic Mark, M.; Molina, H.; Kohsaka, S.; di Giannatale, A.; Ceder, S.; et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015, 527, 329-335.
13. Trajkovic, K.; Hsu, C.; Chiantia, S.; Rajendran, L.; Wenzel, D.; Wieland, F.; Schwille, P.; Brugger, B.; Simons, M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008, 319, 1244-1247.
14. Bradley, E.W.; Carpio, L.R.; vanWijnen, A.J.; McGee-Lawrence, M.E.; Westendorf, J.J. Histone deacetylases in bone development and skeletal disorders. Physiol. Rev. 2015, 95, 1359-1381.
15. Ornitz, D.M.; Marie, P.J. Fgf signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev. 2002, 16, 1446-1465.
16. Kronenberg, H.M. Developmental regulation of the growth plate. Nature 2003, 423, 332-336.
17. Grellier, M.; Bordenave, L.; Amedee, J. Cell-to-cell communication between osteogenic and endothelial lineages: Implications for tissue engineering. Trends Biotechnol. 2009, 27, 562-571.
18. Gerber, H.P.; Vu, T.H.; Ryan, A.M.; Kowalski, J.; Werb, Z.; Ferrara, N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat. Med. 1999, 5, 623-628.
19. Hilton, M.J.; Tu, X.; Wu, X.; Bai, S.; Zhao, H.; Kobayashi, T.; Kronenberg, H.M.; Teitelbaum, S.L.; Ross, F.P.; Kopan, R.; et al. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat. Med. 2008, 14, 306-314.
20. Ramasamy, S.K.; Kusumbe, A.P.; Wang, L.; Adams, R.H. Endothelial notch activity promotes angiogenesis and osteogenesis in bone. Nature 2014, 507, 376-380.
21. Trams, E.G.; Lauter, C.J.; Salem, N., Jr.; Heine, U. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim. Biophys. Acta 1981, 645, 63-70.
22. Van Niel, G.; Porto-Carreiro, I.; Simoes, S.; Raposo, G. Exosomes: A common pathway for a specialized function. J. Biochem. 2006, 140, 13-21.
23. Harding, C.; Heuser, J.; Stahl, P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J. Cell Biol. 1983, 97, 329-339.
24. Pan, B.T.; Johnstone, R.M. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor. Cell 1983, 33, 967-978.
25. Thery, C.; Regnault, A.; Garin, J.; Wolfers, J.; Zitvogel, L.; Ricciardi-Castagnoli, P.; Raposo, G.; Amigorena, S. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J. Cell Biol. 1999, 147, 599-610.
26. Raposo, G.; Nijman, H.W.; Stoorvogel, W.; Liejendekker, R.; Harding, C.V.; Melief, C.J.; Geuze, H.J. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 1996, 183, 1161-1172.
27. Blanchard, N.; Lankar, D.; Faure, F.; Regnault, A.; Dumont, C.; Raposo, G.; Hivroz, C. TCR activation of human t cells induces the production of exosomes bearing the TCR/CD3/complex. J. Immunol. 2002, 168, 3235-3241.
28. Raposo, G.; Tenza, D.; Mecheri, S.; Peronet, R.; Bonnerot, C.; Desaymard, C. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol. Biol. Cell 1997, 8, 2631-2645.
29. Van Niel, G.; Raposo, G.; Candalh, C.; Boussac, M.; Hershberg, R.; Cerf-Bensussan, N.; Heyman, M. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001, 121, 337-349.
30. Mears, R.; Craven, R.A.; Hanrahan, S.; Totty, N.; Upton, C.; Young, S.L.; Patel, P.; Selby, P.J.; Banks, R.E. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 2004, 4, 4019-4031.
31. Valadi, H.; Ekstrom, K.; Bossios, A.; Sjostrand, M.; Lee, J.J.; Lotvall, J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9, 654-659.
32. Taylor, D.D.; Gercel-Taylor, C. Microrna signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 2008, 110, 13-21.
33. Al-Nedawi, K.; Meehan, B.; Micallef, J.; Lhotak, V.; May, L.; Guha, A.; Rak, J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008, 10, 619-624.
34. Luketic, L.; Delanghe, J.; Sobol, P.T.; Yang, P.; Frotten, E.; Mossman, K.L.; Gauldie, J.; Bramson, J.; Wan, Y. Antigen presentation by exosomes released from peptide-pulsed dendritic cells is not suppressed by the presence of active CTL. J. Immunol. 2007, 179, 5024-5032.
35. Balaj, L.; Lessard, R.; Dai, L.; Cho, Y.J.; Pomeroy, S.L.; Breakefield, X.O.; Skog, J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun. 2011, 2, 180.
36. Webber, J.P.; Spary, L.K.; Sanders, A.J.; Chowdhury, R.; Jiang, W.G.; Steadman, R.; Wymant, J.; Jones, A.T.; Kynaston, H.; Mason, M.D.; et al. Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes. Oncogene 2015, 34, 290-302.
37. Yamaguchi, T.; Izumi, Y.; Nakamura, Y.; Yamazaki, T.; Shiota, M.; Sano, S.; Tanaka, M.; Osada-Oka, M.; Shimada, K.; Miura, K.; et al. Repeated remote ischemic conditioning attenuates left ventricular remodeling via exosome-mediated intercellular communication on chronic heart failure after myocardial infarction. Int. J. Cardiol. 2015, 178, 239-246.
38. Denzer, K.; van Eijk, M.; Kleijmeer, M.J.; Jakobson, E.; de Groot, C.; Geuze, H.J. Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J. Immunol. 2000, 165, 1259-1265.
39. Clayton, A.; Turkes, A.; Dewitt, S.; Steadman, R.; Mason, M.D.; Hallett, M.B. Adhesion and signaling by B cell-derived exosomes: The role of integrins. FASEB J. 2004, 18, 977-979.
40. Morelli, A.E.; Larregina, A.T.; Shufesky, W.J.; Sullivan, M.L.; Stolz, D.B.; Papworth, G.D.; Zahorchak, A.F.; Logar, A.J.; Wang, Z.; Watkins, S.C.; et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004, 104, 3257-3266.
41. Koppers-Lalic, D.; Hogenboom, M.M.; Middeldorp, J.M.; Pegtel, D.M. Virus-modified exosomes for targeted rna delivery; a new approach in nanomedicine. Adv. Drug Deliv. Rev. 2013, 65, 348-356.
42. Simpson, R.J.; Jensen, S.S.; Lim, J.W. Proteomic profiling of exosomes: Current perspectives. Proteomics 2008, 8, 4083-4099.
43. Van Dommelen, S.M.; Vader, P.; Lakhal, S.; Kooijmans, S.A.; van Solinge, W.W.; Wood, M.J.; Schiffelers, R.M. Microvesicles and exosomes: Opportunities for cell-derived membrane vesicles in drug delivery. J. Control. Release 2012, 161, 635-644.
44. Gibbings, D.; Voinnet, O. Control of RNA silencing and localization by endolysosomes. Trends Cell Biol. 2010, 20, 491-501.
45. Pegtel, D.M.; Cosmopoulos, K.; Thorley-Lawson, D.A.; van Eijndhoven, M.A.; Hopmans, E.S.; Lindenberg, J.L.; de Gruijl, T.D.; Wurdinger, T.; Middeldorp, J.M. Functional delivery of viral mirnas via exosomes. Proc. Natl. Acad. Sci. USA 2010, 107, 6328-6333.
46. Lee, C.; Mitsialis, S.A.; Aslam, M.; Vitali, S.H.; Vergadi, E.; Konstantinou, G.; Sdrimas, K.; Fernandez-Gonzalez, A.; Kourembanas, S. Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation 2012, 126, 2601-2611.
47. Zhou, Y.; Xu, H.; Xu, W.; Wang, B.; Wu, H.; Tao, Y.; Zhang, B.; Wang, M.; Mao, F.; Yan, Y.; et al. Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro. Stem Cell Res. Ther. 2013, 4, 34.
48. Alvarez-Erviti, L.; Seow, Y.; Yin, H.; Betts, C.; Lakhal, S.; Wood, M.J. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 2011, 29, 341-345.
49. Basu, J.; Ludlow, J.W. Exosomes for repair, regeneration and rejuvenation. Expert Opin. Biol. Ther. 2016, 16, 489-506.
50. Narayanan, R.; Huang, C.C.; Ravindran, S. Hijacking the cellular mail: Exosome mediated differentiation of mesenchymal stem cells. Stem Cells Int. 2016, 2016, 3808674.
51. Xu, J.F.; Yang, G.H.; Pan, X.H.; Zhang, S.J.; Zhao, C.; Qiu, B.S.; Gu, H.F.; Hong, J.F.; Cao, L.; Chen, Y.; et al. Altered microrna expression profile in exosomes during osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. PLoS ONE 2014, 9, e114627.
52. Cui, Y.; Luan, J.; Li, H.; Zhou, X.; Han, J. Exosomes derived from mineralizing osteoblasts promote ST2 cell osteogenic differentiation by alteration of microrna expression. FEBS Lett. 2016, 590, 185-192.
53. Ge, M.; Ke, R.; Cai, T.; Yang, J.; Mu, X. Identification and proteomic analysis of osteoblast-derived exosomes. Biochem. Biophys. Res. Commun. 2015, 467, 27-32.
54. Wang, Z.; Ding, L.; Zheng, X.L.; Wang, H.X.; Yan, H.M. DC-derived exosomes induce osteogenic differentiation of mesenchymal stem cells. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2014, 22, 600-604.
55. Ekstrom, K.; Omar, O.; Graneli, C.; Wang, X.; Vazirisani, F.; Thomsen, P. Monocyte exosomes stimulate the osteogenic gene expression of mesenchymal stem cells. PLoS ONE 2013, 8, e75227.
56. Golub, E.E. Biomineralization and matrix vesicles in biology and pathology. Semin. Immunopathol. 2011, 33, 409-417.
57. Inder, K.L.; Ruelcke, J.E.; Petelin, L.; Moon, H.; Choi, E.; Rae, J.; Blumenthal, A.; Hutmacher, D.; Saunders, N.A.; Stow, J.L.; et al. Cavin-1/PTRF alters prostate cancer cell-derived extracellular vesicle content and internalization to attenuate extracellular vesicle-mediated osteoclastogenesis and osteoblast proliferation. J. Extracell. Vesicles 2014, 3, 23784.
58. Kawakubo, A.; Matsunaga, T.; Ishizaki, H.; Yamada, S.; Hayashi, Y. Zinc as an essential trace element in the acceleration of matrix vesicles-mediated mineral deposition. Microsc. Res. Tech. 2011, 74, 1161-1165.
59. Qin, Y.; Wang, L.; Gao, Z.; Chen, G.; Zhang, C. Bone marrow stromal/stem cell-derived extracellular vesicles regulate osteoblast activity and differentiation in vitro and promote bone regeneration in vivo. Sci. Rep. 2016, 6, 21961.
60. Raimondi, L.; de Luca, A.; Amodio, N.; Manno, M.; Raccosta, S.; Taverna, S.; Bellavia, D.; Naselli, F.; Fontana, S.; Schillaci, O.; et al. Involvement of multiple myeloma cell-derived exosomes in osteoclast differentiation. Oncotarget 2015, 6, 13772-13789.
61. Solberg, L.B.; Stang, E.; Brorson, S.H.; Andersson, G.; Reinholt, F.P. Tartrate-resistant acid phosphatase (TRAP) co-localizes with receptor activator of NF-KB ligand (RANKL) and osteoprotegerin (OPG) in lysosomal-associated membrane protein 1 (LAMP1)-positive vesicles in rat osteoblasts and osteocytes. Histochem. Cell Biol. 2015, 143, 195-207.
62. Huynh, N.; VonMoss, L.; Smith, D.; Rahman, I.; Felemban, M.F.; Zuo, J.; Rody, W.J., Jr.; McHugh, K.P.; Holliday, L.S. Characterization of regulatory extracellular vesicles from osteoclasts. J. Dent. Res. 2016.
63. Salomon, C.; Ryan, J.; Sobrevia, L.; Kobayashi, M.; Ashman, K.; Mitchell, M.; Rice, G.E. Exosomal signaling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis. PLoS ONE 2013, 8, e68451.
64. Janiszewski, M.; Do Carmo, A.O.; Pedro, M.A.; Silva, E.; Knobel, E.; Laurindo, F.R. Platelet-derived exosomes of septic individuals possess proapoptotic NAD(P)H oxidase activity: A novel vascular redox pathway. Crit. Care Med. 2004, 32, 818-825.
65. Vrijsen, K.R.; Sluijter, J.P.; Schuchardt, M.W.; van Balkom, B.W.; Noort, W.A.; Chamuleau, S.A.; Doevendans, P.A. Cardiomyocyte progenitor cell-derived exosomes stimulate migration of endothelial cells. J. Cell. Mol. Med. 2010, 14, 1064-1070.
66. Sahoo, S.; Klychko, E.; Thorne, T.; Misener, S.; Schultz, K.M.; Millay, M.; Ito, A.; Liu, T.; Kamide, C.; Agrawal, H.; et al. Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ. Res. 2011, 109, 724-728.
67. Bian, S.; Zhang, L.; Duan, L.; Wang, X.; Min, Y.; Yu, H. Extracellular vesicles derived from human bone marrow mesenchymal stem cells promote angiogenesis in a rat myocardial infarction model. J. Mol. Med. 2014, 92, 387-397.
68. Zhang, H.C.; Liu, X.B.; Huang, S.; Bi, X.Y.; Wang, H.X.; Xie, L.X.; Wang, Y.Q.; Cao, X.F.; Lv, J.; Xiao, F.J.; et al. Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo. Stem Cells Dev. 2012, 21, 3289-3297.
69. Kordelas, L.; Rebmann, V.; Ludwig, A.K.; Radtke, S.; Ruesing, J.; Doeppner, T.R.; Epple, M.; Horn, P.A.; Beelen, D.W.; Giebel, B. Msc-derived exosomes: A novel tool to treat therapy-refractory graft-versus-host disease. Leukemia 2014, 28, 970-973.
70. Harshyne, L.A.; Nasca, B.J.; Kenyon, L.C.; Andrews, D.W.; Hooper, D.C. Serum exosomes and cytokines promote a T-helper cell type 2 environment in the peripheral blood of glioblastoma patients. Neuro Oncol. 2016, 18, 206-215.
71. Yu, B.; Zhang, X.; Li, X. Exosomes derived from mesenchymal stem cells. Int. J. Mol. Sci. 2014, 15, 4142-4157.
72. Peinado, H.; Aleckovic, M.; Lavotshkin, S.; Matei, I.; Costa-Silva, B.; Moreno-Bueno, G.; Hergueta-Redondo, M.; Williams, C.; Garcia-Santos, G.; Ghajar, C.; et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through met. Nat. Med. 2012, 18, 883-891.
73. Lobb, R.J.; Becker, M.; Wen, S.W.; Wong, C.S.; Wiegmans, A.P.; Leimgruber, A.; Moller, A. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J. Extracell. Vesicles 2015, 4, 27031.
74. Baglio, S.R.; Rooijers, K.; Koppers-Lalic, D.; Verweij, F.J.; Perez Lanzon, M.; Zini, N.; Naaijkens, B.; Perut, F.; Niessen, H.W.; Baldini, N.; et al. Human bone marrow-and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive mirna and trna species. Stem Cell Res. Ther. 2015, 6, 127.
75. Vallabhaneni, K.C.; Penfornis, P.; Dhule, S.; Guillonneau, F.; Adams, K.V.; Mo, Y.Y.; Xu, R.; Liu, Y.; Watabe, K.; Vemuri, M.C.; et al. Extracellular vesicles from bone marrow mesenchymal stem/stromal cells transport tumor regulatory microRNA, proteins, and metabolites. Oncotarget 2015, 6, 4953-4967.
76. Lai, C.P.; Mardini, O.; Ericsson, M.; Prabhakar, S.; Maguire, C.A.; Chen, J.W.; Tannous, B.A.; Breakefield, X.O. Dynamic biodistribution of extracellular vesicles in vivo using a multimodal imaging reporter. ACS Nano 2014, 8, 483-494.
77. Hu, G.W.; Li, Q.; Niu, X.; Hu, B.; Liu, J.; Zhou, S.M.; Guo, S.C.; Lang, H.L.; Zhang, C.Q.; Wang, Y.; et al. Exosomes secreted by human-induced pluripotent stem cell-derived mesenchymal stem cells attenuate limb ischemia by promoting angiogenesis in mice. Stem Cell Res. Ther. 2015, 6, 10.
78. Taverna, S.; Flugy, A.; Saieva, L.; Kohn, E.C.; Santoro, A.; Meraviglia, S.; de Leo, G.; Alessandro, R. Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis. Int. J. Cancer 2012, 130, 2033-2043.
79. Bergers, G.; Benjamin, L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 2003, 3, 401-410.
80. Umezu, T.; Ohyashiki, K.; Kuroda, M.; Ohyashiki, J.H. Leukemia cell to endothelial cell communication via exosomal mirnas. Oncogene 2013, 32, 2747-2755.
81. Lopatina, T.; Bruno, S.; Tetta, C.; Kalinina, N.; Porta, M.; Camussi, G. Platelet-derived growth factor regulates the secretion of extracellular vesicles by adipose mesenchymal stem cells and enhances their angiogenic potential. Cell Commun. Signal. 2014, 12, 26.