How Do Mesenchymal Stem Cells Influence or Are Influenced by Microenvironment through Extracellular Vesicles Communication?

Frontiers in Cell and Developmental Biology

Volumn 5, Issue , 2017, Pages

  Dostert, Gabriel ^a   Mesure, Benjamin ^a   Menu, Patrick ^a   Velot, Émilie ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

Author keywords

extracellular vesicles (EVs); intercellular communication; mesenchymal stem cells (MSCs); microenvironment; recipient donor cells

Indexed keywords

EID: 85020457369     PISSN: None     EISSN: 2296634X     Source Type: Journal    
DOI: 10.3389/fcell.2017.00006     Document Type: Review

References (66)

1. Anderson J. D. Johansson H. J. Graham C. S. Vesterlund M. Pham M. T. Bramlett C. S. et al. (2016). Comprehensive proteomic analysis of mesenchymal stem cell exosomes reveals modulation of angiogenesis via NFκB signaling: MSC exosomes induce angiogenesis via NFκB pathway. Stem Cells. 34, 601–613. 10.1002/stem.229826782178
2. Atkin-Smith G. K. Tixeira R. Paone S. Mathivanan S. Collins C. Liem M. et al. (2015). A novel mechanism of generating extracellular vesicles during apoptosis via a beads-on-a-string membrane structure. Nat. Commun. 6:7439. 10.1038/ncomms843926074490
3. Bian S. Zhang L. Duan L. Wang X. Min Y. Yu H. (2014). Extracellular vesicles derived from human bone marrow mesenchymal stem cells promote angiogenesis in a rat myocardial infarction model. J. Mol. Med. 92, 387–397. 10.1007/s00109-013-1110-524337504
4. Bruno S. Collino F. Deregibus M. C. Grange C. Tetta C. Camussi G. (2013). Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells Dev. 22, 758–771. 10.1089/scd.2012.030423034046
5. Chen T. S. Arslan F. Yin Y. Tan S. S. Lai R. C. Choo A. B. H. et al. (2011). Enabling a robust scalable manufacturing process for therapeutic exosomes through oncogenic immortalization of human ESC-derived MSCs. J. Transl. Med. 9:47. 10.1186/1479-5876-9-4721513579
6. Chiabotto G. Bruno S. Collino F. Camussi G. (2016). Mesenchymal stromal cells epithelial transition induced by renal tubular cells-derived extracellular vesicles. PLoS ONE 11:e0159163. 10.1371/journal.pone.015916327409796
7. Cho J. Park H. Lim E. Lee K. (2011). Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int. J. Oncol. 40, 130–138. 10.3892/ijo.2011.119321904773
8. Chowdhury R. Webber J. P. Gurney M. Mason M. D. Tabi Z. Clayton A. (2015). Cancer exosomes trigger mesenchymal stem cell differentiation into pro-angiogenic and pro-invasive myofibroblasts. Oncotarget 6, 715–731. 10.18632/oncotarget.271125596732
9. Corrado C. Raimondo S. Saieva L. Flugy A. M. De Leo G. Alessandro R. (2014). Exosome-mediated crosstalk between chronic myelogenous leukemia cells and human bone marrow stromal cells triggers an interleukin 8-dependent survival of leukemia cells. Cancer Lett. 348, 71–76. 10.1016/j.canlet.2014.03.00924657661
10. Crescitelli R. Lässer C. Szabó T. G. Kittel A. Eldh M. Dianzani I. et al. (2013). Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J. Extracell. Vesicles 2:20677. 10.3402/jev.v2i0.2067724223256
11. Del Fattore A. Luciano R. Pascucci L. Goffredo B. M. Giorda E. Scapaticci M. et al. (2015). Immunoregulatory effects of mesenchymal stem cell-derived extracellular vesicles on T lymphocytes. Cell Transplant. 24, 2615–2627. 10.3727/096368915X68754325695896
12. Desando G. Giavaresi G. Cavallo C. Bartolotti I. Sartoni F. Nicoli Aldini N. et al. (2016). Autologous bone marrow concentrate in a sheep model of osteoarthritis: new perspectives for cartilage and meniscus repair. Tissue Eng. C Methods 22, 608–619. 10.1089/ten.TEC.2016.003327151837
13. Di Trapani M. Bassi G. Midolo M. Gatti A. Kamga P. T. Cassaro A. et al. (2016). Differential and transferable modulatory effects of mesenchymal stromal cell-derived extracellular vesicles on T, B and NK cell functions. Sci. Rep. 6:24120. 10.1038/srep2412027071676
14. Ekström K. Omar O. Granéli C. Wang X. Vazirisani F. Thomsen P. (2013). Monocyte Exosomes stimulate the osteogenic gene expression of mesenchymal stem cells. PLoS ONE 8:e75227. 10.1371/journal.pone.007522724058665
15. El Omar R. Beroud J. Stoltz J.-F. Menu P. Velot E. Decot V. (2014). Umbilical cord mesenchymal stem cells: the new gold standard for mesenchymal stem cell-based therapies? Tissue Eng. B Rev. 20, 523–544. 10.1089/ten.TEB.2013.066424552279
16. Feng Y. Huang W. Wani M. Yu X. Ashraf M. (2014). Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22. PLoS ONE 9:e88685. 10.1371/journal.pone.008868524558412
17. Goloviznina N. A. Verghese S. C. Yoon Y. M. Taratula O. Marks D. L. Kurre P. (2016). Mesenchymal stromal cell-derived extracellular vesicles promote myeloid-biased multipotent hematopoietic progenitor expansion via toll-like receptor engagement. J. Biol. Chem. 291, 24607–24617. 10.1074/jbc.M116.74565327758863
18. György B. Szabó T. G. Pásztói M. Pál Z. Misják P. Aradi B. et al. (2011). Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell. Mol. Life Sci. 68, 2667–2688. 10.1007/s00018-011-0689-321560073
19. Haga H. Yan I. K. Takahashi K. Wood J. Zubair A. Patel T. (2015). Tumour cell–derived extracellular vesicles interact with mesenchymal stem cells to modulate the microenvironment and enhance cholangiocarcinoma growth. J. Extracell. Vesicles 4:24900. 10.3402/jev.v4.2490025557794
20. Hendijani F. Javanmard S. H. Rafiee L. Sadeghi-Aliabadi H. (2015). Effect of human Wharton's jelly mesenchymal stem cell secretome on proliferation, apoptosis and drug resistance of lung cancer cells. Res. Pharm. Sci. 10, 134–142. 26487890
21. Hofer H. R. Tuan R. S. (2016). Secreted trophic factors of mesenchymal stem cells support neurovascular and musculoskeletal therapies. Stem Cell Res. Ther. 7:131. 10.1186/s13287-016-0394-027612948
22. Höög J. L. Lötvall J. (2015). Diversity of extracellular vesicles in human ejaculates revealed by cryo-electron microscopy. J. Extracell. Vesicles 4:28680. 10.3402/jev.v4.2868026563734
23. Introna M. Lucchini G. Dander E. Galimberti S. Rovelli A. Balduzzi A. et al. (2014). Treatment of graft versus host disease with mesenchymal stromal cells: a phase I study on 40 adult and pediatric patients. Biol. Blood Marrow Transplant. 20, 375–381. 10.1016/j.bbmt.2013.11.03324321746
24. Ji R. Zhang B. Zhang X. Xue J. Yuan X. Yan Y. et al. (2015). Exosomes derived from human mesenchymal stem cells confer drug resistance in gastric cancer. Cell Cycle 14, 2473–2483. 10.1080/15384101.2015.100553026091251
25. Johnsen K. B. Gudbergsson J. M. Skov M. N. Pilgaard L. Moos T. Duroux M. (2014). A comprehensive overview of exosomes as drug delivery vehicles — Endogenous nanocarriers for targeted cancer therapy. Biochim. Biophys. Acta 1846, 75–87. 10.1016/j.bbcan.2014.04.00524747178
26. Katakowski M. Buller B. Zheng X. Lu Y. Rogers T. Osobamiro O. et al. (2013). Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett. 335, 201–204. 10.1016/j.canlet.2013.02.01923419525
27. Ke F. Zhang L. Liu Z. Yan S. Xu Z. Bai J. et al. (2016). Soluble tumor necrosis factor receptor 1 released by skin-derived mesenchymal stem cells is critical for inhibiting Th17 cell differentiation: sTNFR1 inhibited Th17 cell differentiation. Stem Cells Transl. Med. 5, 301–313. 10.5966/sctm.2015-017926819253
28. Kerkelä E. Laitinen A. Räbinä J. Valkonen S. Takatalo M. Larjo A. et al. (2016). Adenosinergic immunosuppression by human mesenchymal stromal cells requires co-operation with T cells: adenosinergic immunosuppression by human MSCs. Stem Cells 34, 781–790. 10.1002/stem.228026731338
29. Kordelas L. Rebmann V. Ludwig A.-K. Radtke S. Ruesing J. Doeppner T. R. et al. (2014). MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus-host disease. Leukemia 28, 970–973. 10.1038/leu.2014.4124445866
30. Kowal J. Arras G. Colombo M. Jouve M. Morath J. P. Primdal-Bengtson B. et al. (2016). Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc. Natl. Acad. Sci. U.S.A. 113, E968–E977. 10.1073/pnas.152123011326858453
31. Le Blanc K. Frassoni F. Ball L. Locatelli F. Roelofs H. Lewis I. et al. (2008). Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371, 1579–1586. 10.1016/S0140-6736(08)60690-X18468541
32. Lee J.-K. Park S.-R. Jung B.-K. Jeon Y.-K. Lee Y.-S. Kim M.-K. et al. (2013). Exosomes Derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PLoS ONE 8:e84256. 10.1371/journal.pone.008425624391924
33. Li T. Yan Y. Wang B. Qian H. Zhang X. Shen L. et al. (2013). Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev. 22, 845–854. 10.1089/scd.2012.039523002959
34. Li X. Wang S. Zhu R. Li H. Han Q. Zhao R. C. (2016). Lung tumor exosomes induce a pro-inflammatory phenotype in mesenchymal stem cells via NFκB-TLR signaling pathway. J. Hematol. Oncol. 9:42. 10.1186/s13045-016-0269-y27090786
35. Lindoso R. S. Collino F. Camussi G. (2015). Extracellular vesicles derived from renal cancer stem cells induce a pro-tumorigenic phenotype in mesenchymal stromal cells. Oncotarget 6:7959. 10.18632/oncotarget.350325797265
36. Lopatina T. Gai C. Deregibus M. C. Kholia S. Camussi G. (2016). Cross talk between cancer and mesenchymal stem cells through extracellular vesicles carrying nucleic acids. Front. Oncol. 6:125. 10.3389/fonc.2016.0012527242964
37. Lou G. Song X. Yang F. Wu S. Wang J. Chen Z. et al. (2015). Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma. J. Hematol. Oncol. 8:122. 10.1186/s13045-015-0220-726514126
38. Lozito T. P. Tuan R. S. (2014). Endothelial and cancer cells interact with mesenchymal stem cells via both microparticles and secreted factors. J. Cell. Mol. Med. 18, 2372–2384. 10.1111/jcmm.1239125250510
39. Martins M. Ribeiro D. Martins A. Reis R. L. Neves N. M. (2016). Extracellular vesicles derived from osteogenically induced human bone marrow mesenchymal stem cells can modulate lineage commitment. Stem Cell Rep. 6, 284–291. 10.1016/j.stemcr.2016.01.00126923821
40. Melief S. M. Schrama E. Brugman M. H. Tiemessen M. M. Hoogduijn M. J. Fibbe W. E. et al. (2013). Multipotent stromal cells induce human regulatory T cells through a novel pathway involving skewing of monocytes toward anti-inflammatory macrophages: MSC induce tregs through skewing of monocytes. Stem Cells 31, 1980–1991. 10.1002/stem.143223712682
41. Mendicino M. Bailey A. M. Wonnacott K. Puri R. K. Bauer S. R. (2014). MSC-based product characterization for clinical trials: an FDA perspective. Cell Stem Cell 14, 141–145. 10.1016/j.stem.2014.01.01324506881
42. Montemurro T. Viganò M. Ragni E. Barilani M. Parazzi V. Boldrin V. et al. (2016). Angiogenic and anti-inflammatory properties of mesenchymal stem cells from cord blood: soluble factors and extracellular vesicles for cell regeneration. Eur. J. Cell Biol. 95, 228–238. 10.1016/j.ejcb.2016.04.00327139721
43. Nakamura Y. Miyaki S. Ishitobi H. Matsuyama S. Nakasa T. Kamei N. et al. (2015). Mesenchymal-stem-cell-derived exosomes accelerate skeletal muscle regeneration. FEBS Lett. 589, 1257–1265. 10.1016/j.febslet.2015.03.03125862500
44. Omar O. M. Granéli C. Ekström K. Karlsson C. Johansson A. Lausmaa J. et al. (2011). The stimulation of an osteogenic response by classical monocyte activation. Biomaterials 32, 8190–8204. 10.1016/j.biomaterials.2011.07.05521835463
45. Paggetti J. Haderk F. Seiffert M. Janji B. Distler U. Ammerlaan W. et al. (2015). Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 126, 1106–1117. 10.1182/blood-2014-12-61802526100252
46. Ratajczak J. Wysoczynski M. Hayek F. Janowska-Wieczorek A. Ratajczak M. Z. (2006). Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487–1495. 10.1038/sj.leu.240429616791265
47. Roccaro A. M. Sacco A. Maiso P. Azab A. K. Tai Y.-T. Reagan M. et al. (2013). BM mesenchymal stromal cell–derived exosomes facilitate multiple myeloma progression. J. Clin. Invest. 123, 1542–1555. 10.1172/JCI6651723454749
48. Sattayaprasert P. Nassal D. M. Wan X. Deschenes I. Laurita K. R. (2016). Mesenchymal stem cells suppress cardiac alternans by activation of PI3K mediated nitroso-redox pathway. J. Mol. Cell. Cardiol. 98, 138–145. 10.1016/j.yjmcc.2016.05.01427238412
49. Shi S. Zhang Q. Xia Y. You B. Shan Y. Bao L. et al. (2016). Mesenchymal stem cell-derived exosomes facilitate nasopharyngeal carcinoma progression. Am. J. Cancer Res. 6:459. 27186416
50. Si Y.-L. Zhao Y.-L. Hao H.-J. Fu X.-B. Han W.-D. (2011). MSCs: Biological characteristics, clinical applications and their outstanding concerns. Ageing Res. Rev. 10, 93–103. 10.1016/j.arr.2010.08.00520727988
51. Takeda Y. S. Xu Q. (2015). Neuronal Differentiation of Human Mesenchymal stem cells using exosomes derived from differentiating neuronal cells. PLOS ONE 10:e0135111. 10.1371/journal.pone.013511126248331
52. Teng X. Chen L. Chen W. Yang J. Yang Z. Shen Z. (2015). Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation. Cell. Physiol. Biochem. 37, 2415–2424. 10.1159/00043859426646808
53. Ti D. Hao H. Tong C. Liu J. Dong L. Zheng J. et al. (2015). LPS-preconditioned mesenchymal stromal cells modify macrophage polarization for resolution of chronic inflammation via exosome-shuttled let-7b. J. Transl. Med. 13:308. 10.1186/s12967-015-0642-626386558
54. Valadi H. Ekström K. Bossios A. Sjöstrand M. Lee J. J. Lötvall J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654–659. 10.1038/ncb159617486113
55. Vlassov A. V. Magdaleno S. Setterquist R. Conrad R. (2012). Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta 1820, 940–948. 10.1016/j.bbagen.2012.03.01722503788
56. Wang X. Gu H. Qin D. Yang L. Huang W. Essandoh K. et al. (2015). Exosomal miR-223 contributes to mesenchymal stem cell-elicited cardioprotection in polymicrobial sepsis. Sci. Rep. 5:13721. 10.1038/srep1372126348153
57. Xin H. Li Y. Cui Y. Yang J. J. Zhang Z. G. Chopp M. (2013). Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. J. Cereb. Blood Flow Metab. 33, 1711–1715. 10.1038/jcbfm.2013.15223963371
58. Xing L. Cui R. Peng L. Ma J. Chen X. Xie R.-J. et al. (2014). Mesenchymal stem cells, not conditioned medium, contribute to kidney repair after ischemia-reperfusion injury. Stem Cell Res Ther 5:101. 10.1186/scrt48928097053
59. Yáñez-Mó M. Siljander P. R.-M. Andreu Z. Bedina Zavec A. Borràs F. E. Buzas E. I. et al. (2015). Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles 4:27066. 10.3402/jev.v4.2706625979354
60. Yang Y. Bucan V. Baehre H. von der Ohe J. Otte A. Hass R. (2015). Acquisition of new tumor cell properties by MSC-derived exosomes. Int. J. Oncol. 47, 244–252. 10.3892/ijo.2015.300125963929
61. Yu B. Kim H. W. Gong M. Wang J. Millard R. W. Wang Y. et al. (2015). Exosomes secreted from GATA-4 overexpressing mesenchymal stem cells serve as a reservoir of anti-apoptotic microRNAs for cardioprotection. Int. J. Cardiol. 182, 349–360. 10.1016/j.ijcard.2014.12.04325590961
62. Zhang B. Yin Y. Lai R. C. Tan S. S. Choo A. B. H. Lim S. K. (2014). Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells Dev. 23, 1233–1244. 10.1089/scd.2013.047924367916
63. Zhang J. Guan J. Niu X. Hu G. Guo S. Li Q. et al. (2015). Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis. J. Transl. Med. 13:49. 10.1186/s12967-015-0417-025638205
64. Zhang J. Liu X. Li H. Chen C. Hu B. Niu X. et al. (2016). Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway. Stem Cell Res. Ther. 7:136. 10.1186/s13287-016-0391-327650895
65. Zhou H. Guo M. Bian C. Sun Z. Yang Z. Zeng Y. et al. (2010). Efficacy of bone marrow-derived mesenchymal stem cells in the treatment of sclerodermatous chronic graft-versus-host disease: clinical report. Biol. Blood Marrow Transplant. 16, 403–412. 10.1016/j.bbmt.2009.11.00619925878
66. Zhu Y. Feng X. Abbott J. Fang X. Hao Q. Monsel A. et al. (2014). Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice: MSC MV attenuates ALI in part through, KGF. Stem cells 32, 116–125. 10.1002/stem.150423939814