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Extracellular Vesicles and Prospects of Their Use for Tissue Regeneration

  • O. N. Sheveleva
  • E. I. Domaratskaya
  • O. V. PayushinaEmail author
REVIEWS

Abstract

Extracellular vesicles are an important component of different cell secretomes that provide complex delivery of biologically active molecules and horizontal transfer of genetic information. They differ in their origin, composition, and functions. Selection of the vesicle isolation protocol, change in the cultivation conditions of the cells producing them and genetic modification influence the composition of the vesicles obtained. Stem cells produce vesicles carrying a wide range of growth factors, chemokines, cytokines, miRNAs that can affect the surrounding cells and have a therapeutic effect in various pathologies. The nature of biogenesis of extracellular vesicles, as well as their effects on target cells, is an important issue of fundamental biology, and improvement of methods for obtaining vesicles of the required composition opens broad prospects for their use in clinical practice.

Keywords:

extracellular vesicles exosomes microvesicles stem cells regeneration 

Notes

ACKNOWLEDGMENTS

The review was prepared within the framework of the Government Basic Research Program of the Presidium of Russian Academy of Sciences no. 42 “Fundamental research for the development of medical technologies”, section of the State task no. 0108-2018-0013.

COMPLIANCE WITH ETHICAL STANDARDS

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

REFERENCES

  1. 1.
    Tibbetts M.D., Samuel M.A., Chang T.S., Ho A.C. 2012. Stem cell therapy for retinal disease. Curr. Opin. Ophthalmol. 23 (3), 226–234.CrossRefGoogle Scholar
  2. 2.
    Martínez-Morales P.L., Revilla A., Ocana I., González C., Sainz P., McGuire D., Liste I. 2013. Progress in stem cell therapy for major human neurological disorders. Stem Cell Rev. 9 (5), 685–699.CrossRefGoogle Scholar
  3. 3.
    Sanganalmath S.K., Bolli R. 2013. Cell therapy for heart failure: A comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ. Res. 113 (6), 810–834.CrossRefGoogle Scholar
  4. 4.
    Angelos M.G., Kaufman D.S. 2015. Pluripotent stem cell applications for regenerative medicine. Curr. Opin. Organ Transplant. 20 (6), 663–670.Google Scholar
  5. 5.
    Tolar J., Nauta A.J., Osborn M.J., Panoskaltsis Mortari A., McElmurry R.T., Bell S., Xia L., Zhou N., Riddle M., Schroeder T.M., Westendorf J.J., McIvor R.S., Hogendoorn P.C., Szuhai K., Oseth L., Hirsch B., Yant S.R., Kay M.A., Peister A., Prockop D.J., Fibbe W.E., Blazar B.R. 2007. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells. 25 (2), 371–379.CrossRefGoogle Scholar
  6. 6.
    Tang D.Q., Wang Q., Burkhardt B.R., Litherland S.A., Atkinson M.A., Yang L.J. 2012. In vitro generation of functional insulin-producing cells from human bone marrow-derived stem cells, but long-term culture running risk of malignant transformation. Am. J. Stem Cells. 1 (2), 114–127.Google Scholar
  7. 7.
    de Almeida P.E., Ransohoff J.D., Nahid A., Wu J.C. 2013. Immunogenicity of pluripotent stem cells and their derivatives. Circ. Res. 112 (3), 549–561.CrossRefGoogle Scholar
  8. 8.
    Zhu K., Wu Q., Ni C., Zhang P., Zhong Z., Wu Y., Wang Y., Xu Y., Kong M., Cheng H., Tao Z., Yang Q., Liang H., Jiang Y., Li Q., Zhao J., Huang J., Zhang F., Chen Q., Li Y., Chen J., Zhu W., Yu H., Zhang J., Yang H.T., Hu X., Wang J. 2018. Lack of remuscularization following transplantation of human embryonic stem cell-derived cardiovascular progenitor cells in infarcted nonhuman primates. Circ. Res. 122 (7), 958–969.CrossRefGoogle Scholar
  9. 9.
    Tran C., Damaser M.S. 2015. Stem cells as drug delivery methods: Application of stem cell secretome for regeneration. Adv. Drug Deliv. Rev. 82–83, 1–11.CrossRefGoogle Scholar
  10. 10.
    van der Pol E., Boing A.N., Harrison P., Sturk A., Nieuwland R. 2012. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol. Rev. 64 (3), 676–705.CrossRefGoogle Scholar
  11. 11.
    Johnstone R.M., Adam M., Hammond J.R., Orr L., Turbide C. 1987. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 262 (19), 9412–9420.Google Scholar
  12. 12.
    Théry C., Ostrowski M., Segura E. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9 (8), 581–593.CrossRefGoogle Scholar
  13. 13.
    Gould S.J., Raposo G. 2013. As we wait: Coping with an imperfect nomenclature for extracellular vesicles. J. Extracell. Vesicles. 2. doi  https://doi.org/10.3402/jev.v2i0.20389
  14. 14.
    Yáñez-Mó M., Siljander P.R., Andreu Z., Zavec A.B., Borràs F.E., Buzas E.I., Buzas K., Casal E., Cappello F., Carvalho J., Colás E., Cordeiro-da Silva A., Fais S., Falcon-Perez J.M., Ghobrial I.M., Giebel B., Gimona M., Graner M., Gursel I., Gursel M., Heegaard N.H., Hendrix A., Kierulf P., Kokubun K., Kosanovic M., Kralj-Iglic V., Krämer-Albers E.M., Laitinen S., Lässer C., Lener T., Ligeti E., Linē A., Lipps G., Llorente A., Lötvall J., Manček-Keber M., Marcilla A., Mittelbrunn M., Nazarenko I., Nolte-’t Hoen E.N., Nyman T.A., O’Driscoll L., Olivan M., Oliveira C., Pállinger É., Del Portillo H.A., Reventós J., Rigau M., Rohde E., Sammar M., Sánchez-Madrid F., Santarém N., Schallmoser K., Ostenfeld M.S., Stoorvogel W., Stukelj R., Van der Grein S.G., Vasconcelos M.H., Wauben M.H., De Wever O. 2015. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles. 4. doi  https://doi.org/10.3402/jev.v4.27066
  15. 15.
    van Niel G., D’Angelo G., Raposo G. 2018. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol. 19 (4), 213–228.CrossRefGoogle Scholar
  16. 16.
    Harding C., Heuser J., Stahl P. 1983. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J. Cell Biol. 97 (2), 329–339.CrossRefGoogle Scholar
  17. 17.
    Akers J.C., Gonda D., Kim R., Carter B.S., Chen C.C. 2013. Biogenesis of extracellular vesicles (EV): Exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J. Neurooncol. 113 (1), 1–11.CrossRefGoogle Scholar
  18. 18.
    Muralidharan-Chari V., Clancy J., Plou C., Romao M., Chavrier P., Raposo G., D’Souza-Schorey C. 2009. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr. Biol. 19 (22), 1875–1885.CrossRefGoogle Scholar
  19. 19.
    Tchevkina E.M., Shcherbakov A.M., Zhuravskaya A.Yu., Semina S.E., Komel’kov A.V., Krasil‘nikov M.A. 2015. Exosomes and transfer of (epi)genetic information by tumor cells. Uspekhi Molek. Onkol. (Rus.). 2 (3), 8–20.Google Scholar
  20. 20.
    Tamkovich, S. N., Tutanov O. S., Laktionov P. P. 2016. Exosomes: Generation, structure, transport, biological activity, and diagnostic application. Biochem. (Moscow) Suppl. Series A: Membr. Cell Biol. 10 (3), 163–173.Google Scholar
  21. 21.
    Frydrychowicz M., Kolecka-Bednarczyk A., Madejczyk M., Yasar S., Dworacki G. 2015. Exosomes – structure, biogenesis and biological role in non-small-cell lung cancer. Scand. J. Immunol. 81 (1), 2–10.CrossRefGoogle Scholar
  22. 22.
    Colombo M., Moita C., van Niel G., Kowal J., Vigneron J., Benaroch P., Manel N., Moita L.F., Théry C., Raposo G. 2013. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell. Sci. 126 (Pt 24), 5553–5565.CrossRefGoogle Scholar
  23. 23.
    Colombo M., Raposo G., Thery C. 2014. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30, 255–289.CrossRefGoogle Scholar
  24. 24.
    Carayon K., Chaoui K., Ronzier E. 2011. Proteolipidic composition of exosomes changes during reticulocyte maturation. J. Biol. Chem. 286 (39), 34426–3439.CrossRefGoogle Scholar
  25. 25.
    Kalra H., Drummen G.P., Mathivanan S. 2016. Focus on extracellular vesicles: Introducing the next small big thing. Int. J. Mol. Sci. 17 (2), 170.CrossRefGoogle Scholar
  26. 26.
    Subra C., Laulagnier K., Perret B., Record M. 2007. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie. 89 (2), 205–212.CrossRefGoogle Scholar
  27. 27.
    Iraci N., Leonardi T., Gessler F., Vega B., Pluchino S. 2016. Focus on extracellular vesicles: Physiological role and signalling properties of extracellular membrane vesicles. Int. J. Mol. Sci. 17 (2), 171. doi  https://doi.org/10.3390/ijms17020171 CrossRefGoogle Scholar
  28. 28.
    Luga V., Zhang L., Viloria-Petit A.M., Ogunjimi A.A., Inanlou M.R., Chiu E., Buchanan M., Hosein A.N., Basik M., Wrana J.L. 2012. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell. 151 (7), 1542–1556.CrossRefGoogle Scholar
  29. 29.
    Andreu Z., Yanez-Mo M. 2014. Tetraspanins in extracellular vesicle formation and function. Front. Immunol. 5, 442.CrossRefGoogle Scholar
  30. 30.
    Simpson R.J., Jensen S.S., Lim J.W. 2008. Proteomic profiling of exosomes: Current perspectives. Proteomics. 8 (19), 4083–4099.CrossRefGoogle Scholar
  31. 31.
    Tauro B.J., Greening D.W., Mathias R.A. 2013. Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol. Cell Proteomics. 12 (3), 587–598.CrossRefGoogle Scholar
  32. 32.
    Keerthikumar S., Gangoda L., Liem M., Fonseka P., Atukorala I., Ozcitti C., Mechler A., Adda C.G., Ang C.S., Mathivanan S. 2015. Proteogenomic analysis reveals exosomes are more oncogenic than ectosomes. Oncotarget. 6 (17), 15 375–15 396.CrossRefGoogle Scholar
  33. 33.
    Ahadi A., Khoury S., Losseva M. 2016. A comparative analysis of lncRNAs in prostate cancer exosomes and their parental cell line. Genom Data. 9, 7–9.CrossRefGoogle Scholar
  34. 34.
    Kuwabara Y., Ono K., Horie T., Nishi H., Nagao K., Kinoshita M., Watanabe S., Baba O., Kojima Y., Shizuta S., Imai M., Tamura T., Kita T., Kimura T. 2011. Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate myocardial damage. Circ. Cardiovasc. Genet. 4 (4), 446–454.CrossRefGoogle Scholar
  35. 35.
    Gheytanchi E., Madjd Z., Janani L., Rasti A., Ghods R., Atyabi F., Asadi-Lari M.H., Babashah S. 2017. Exosomal microRNAs as potential circulating biomarkers in gastrointestinal tract cancers: a systematic review protocol. Syst. Rev. 6 (1), 228.CrossRefGoogle Scholar
  36. 36.
    Goto T., Fujiya M., Konishi H., Sasajima J., Fujibayashi S., Hayashi A., Utsumi T., Sato H., Iwama T., Ijiri M., Sakatani A., Tanaka K., Nomura Y., Ueno N., Kashima S., Moriichi K., Mizukami Y., Kohgo Y., Okumura T. 2018. An elevated expression of serum exosomal microRNA-191, -21, -451a of pancreatic neoplasm is considered to be efficient diagnostic marker. BMC Cancer. 18 (1), 116. doi  https://doi.org/10.1186/s12885-018-4006-5 CrossRefGoogle Scholar
  37. 37.
    Lunavat T.R., Cheng L., Kim D.K. 2015. Small RNA deep sequencing discriminates subsets of extracellular vesicles released by melanoma cells–Evidence of unique microRNA cargos. RNA Biol. 12 (8), 810–823.CrossRefGoogle Scholar
  38. 38.
    Théry C., Amigorena S., Raposo G. 2006. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chapter 3, Unit 3.22.Google Scholar
  39. 39.
    Momen-Heravi F., Balaj L., Alian S., Mantel P.Y., Halleck A.E., Trachtenberg A.J., Soria C.E., Oquin S., Bonebreak C.M., Saracoglu E., Skog J., Kuo W.P. 2013. Current methods for the isolation of extracellular vesicles. Biol. Chem. 394 (10), 1253–1262.CrossRefGoogle Scholar
  40. 40.
    Greening D.W., Xu R., Ji H., Tauro B.J., Simpson R.J. 2015. A protocol for exosome isolation and characterization: Evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods Mol. Biol. 1295, 179–209.CrossRefGoogle Scholar
  41. 41.
    Korgel B.A., van Zanten J.H., Monbouquette H.G. 1998. Vesicle size distributions measured by flow field-flow fractionation coupled with multiangle light scattering. Biophys. J. 74 (6), 3264–3272.CrossRefGoogle Scholar
  42. 42.
    Rekker K., Saare M., Roost A.M. 2014. Comparison of serum exosome isolation methods for microRNA profiling. Clin. Biochem. 47 (1–2), 135–138.CrossRefGoogle Scholar
  43. 43.
    Gudbergsson J.M., Johnsen K.B., Skov M.N. 2016. Systematic review of factors influencing extracellular vesicle yield from cell cultures. Cytotechnology. 68 (4), 579–592.CrossRefGoogle Scholar
  44. 44.
    Muntión S., Ramos T.L., Diez-Campelo M., Rosón B., Sánchez-Abarca L.I., Misiewicz-Krzeminska I., Preciado S., Sarasquete M.E., de Las Rivas J., González M., Sánchez-Guijo F., Del Cañizo M.C. 2016. Microvesicles from mesenchymal stromal cells are involved in HPC-microenvironment crosstalk in myelodysplastic patients. PLoS One. 11 (2), e0146722.CrossRefGoogle Scholar
  45. 45.
    Shtam T.A., Burdakov V.S., Landa S.B., Naryzhny S.N., Bairamukov V.Y., Malek A.V., Orlov Y.N., Filatov M.V. 2017. Aggregation by lectins as an approach for exosome isolation from biological fluids: Validation for proteomic studies. Cell and Tissue Biology. 11 (2), 172–179.CrossRefGoogle Scholar
  46. 46.
    Wahlgren J., De L Karlson T., Brisslert M., Vaziri Sani F., Telemo E., Sunnerhagen P., Valadi H. 2012. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucl. Acids Res. 40 (17), e130.CrossRefGoogle Scholar
  47. 47.
    Lamichhane T.N., Raiker R.S., Jay S.M. 2015. Exogenous DNA loading into extracellular vesicles via electroporation is size-dependent and enables limited gene delivery. Mol. Pharm. 12 (10), 3650–3657.CrossRefGoogle Scholar
  48. 48.
    Clayton A., Turkes A., Navabi H., Mason M.D., Tabi Z. 2005. Induction of heat shock proteins in B-cell exosomes. J. Cell. Sci. 118 (Pt 16), 3631–3638.CrossRefGoogle Scholar
  49. 49.
    Lopatina T., Bruno S., Tetta C., Kalinina N., Porta M., Camussi G. 2014. Platelet-derived growth factor regulates the secretion of extracellular vesicles by adipose mesenchymal stem cells and enhances their angiogenic potential. Cell. Commun. Signal. 12, 26.CrossRefGoogle Scholar
  50. 50.
    Ti D., Hao H., Tong C., Liu J., Dong L., Zheng J., Zhao Y., Liu H., Fu X., Han W. 2015. LPS-preconditioned mesenchymal stromal cells modify macrophage polarization for resolution of chronic inflammation via exosome-shuttled let-7b. J. Transl. Med. 13, 308.CrossRefGoogle Scholar
  51. 51.
    Ma J., Zhao Y., Sun L., Sun X., Zhao X., Sun X., Qian H., Xu W., Zhu W. 2017. Exosomes derived from akt-modified human umbilical cord mesenchymal stem cells improve cardiac regeneration and promote angiogenesis via activating platelet-derived growth factor D. Stem Cells Transl. Med. 6 (1), 51–59.CrossRefGoogle Scholar
  52. 52.
    Salomon C., Ryan J., Sobrevia L., Kobayashi M., Ashman K., Mitchell M., Rice G.E. 2013. Exosomal signaling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis. PLoS One. 8 (7), e68451.CrossRefGoogle Scholar
  53. 53.
    Alcayaga-Miranda F., Varas-Godoy M., Khoury M. 2016. Harnessing the angiogenic potential of stem cell-derived exosomes for vascular regeneration. Stem Cells Int. 2016, 3409169.CrossRefGoogle Scholar
  54. 54.
    Xu S., Wang J., Ding N., Hu W., Zhang X., Wang B., Hua J., Wei W., Zhu Q. 2015. Exosome-mediated microRNA transfer plays a role in radiation-induced bystander effect. RNA Biol. 12 (12), 355–1363.Google Scholar
  55. 55.
    Eldh M., Ekström K., Valadi H., Sjöstrand M., Olsson B., Jernås M., Lötvall J. 2010. Exosomes communicate protective messages during oxidative stress; Possible role of exosomal shuttle RNA. PLoS One. 5 (12), e15353.CrossRefGoogle Scholar
  56. 56.
    Borges F.T., Melo S.A., Özdemir B.C., Kato N., Revuelta I., Miller C.A., Gattone V.H. 2nd, LeBleu V.S., Kalluri R. 2013. TGF-β1–containing exosomes from injured epithelial cells activate fibroblasts to initiate tissue regenerative responses and fibrosis. J. Am. Soc. Nephrol. 24 (3), 385–392.CrossRefGoogle Scholar
  57. 57.
    Ekström E.J., Bergenfelz C., von Bülow V., Serifler F., Carlemalm E., Jönsson G., Andersson T., Leandersson K. 2014. WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells. Mol. Cancer. 13, 88.CrossRefGoogle Scholar
  58. 58.
    de Jong O.G., Verhaar M.C., Chen Y., Vader P., Gremmels H., Posthuma G., Schiffelers R.M., Gucek M., van Balkom B.W. 2012. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J. Extracell. Vesicles. 1. doi  https://doi.org/10.3402/jev.v1i0.18396
  59. 59.
    Li J., Liu K., Liu Y., Xu Y., Zhang F., Yang H., Liu J., Pan T., Chen J., Wu M., Zhou X., Yuan Z. 2013. Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity. Nat. Immunol. 14 (8), 793–803.CrossRefGoogle Scholar
  60. 60.
    Crisostomo P.R., Wang Y., Markel T.A., Wang M., Lahm T., Meldrum D.R. 2008. Human mesenchymal stem cells stimulated by TNF-alpha, LPS, or hypoxia produce growth factors by an NF kappa B- but not JNK-dependent mechanism. Am. J. Physiol. Cell Physiol. 294 (3), 675–682.CrossRefGoogle Scholar
  61. 61.
    Yao Y., Zhang F., Wang L., Zhang G., Wang Z., Chen J., Gao X. 2009. Lipopolysaccharide preconditioning enhances the efficacy of mesenchymal stem cells transplantation in a rat model of acute myocardial infarction. J. Biomed. Sci. 16 (1), 74.CrossRefGoogle Scholar
  62. 62.
    Han C., Sun X., Liu L., Jiang H., Shen Y., Xu X., Li J., Zhang G., Huang J., Lin Z., Xiong N., Wang T. 2016. Exosomes and their therapeutic potentials of stem cells. Stem Cells Int. 2016, 7653489.Google Scholar
  63. 63.
    Desrochers L.M., Bordeleau F., Reinhart-King C.A., Cerione R.A., Antonyak M.A. 2016. Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat. Commun. 7, 11958.CrossRefGoogle Scholar
  64. 64.
    Ratajczak J., Miekus K., Kucia M. 2006. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 20 (5), 847–856.CrossRefGoogle Scholar
  65. 65.
    Khan M., Nickoloff E., Abramova T., Johnson J., Verma S.K., Krishnamurthy P., Mackie A.R., Vaughan E., Garikipati V.N., Benedict C., Ramirez V., Lambers E., Ito A., Gao E., Misener S., Luongo T., Elrod J., Qin G., Houser S.R., Koch W.J., Kishore R. 2015. Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ. Res. 117 (1), 52–64.CrossRefGoogle Scholar
  66. 66.
    Yuan A., Farber E.L., Rapoport A.L., Tejada D., Deniskin R., Akhmedov N.B., Farber D.B. 2009. Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One. 4 (3), e4722.CrossRefGoogle Scholar
  67. 67.
    Katsman D., Stackpole E.J., Domin D.R., Farber D.B. 2012. Embryonic stem cell-derived microvesicles induce gene expression changes in Müller cells of the retina. PLoS One. 7 (11), e50417.CrossRefGoogle Scholar
  68. 68.
    Bobis-Wozowicz S., Kmiotek K., Sekula M., Kedracka-Krok S., Kamycka E., Adamiak M., Jankowska U., Madetko-Talowska A., Sarna M., Bik-Multanowski M., Kolcz J., Boruczkowski D., Madeja Z., Dawn B., Zuba-Surma E.K. 2015. Human induced pluripotent stem cell-derived microvesicles transmit RNAs and proteins to recipient mature heart cells modulating cell fate and behavior. Stem Cells. 33 (9), 2748–2761.CrossRefGoogle Scholar
  69. 69.
    Lai R.C., Yeo R.W., Lim S.K. 2015. Mesenchymal stem cell exosomes. Semin. Cell Dev. Biol. 40, 82–88.CrossRefGoogle Scholar
  70. 70.
    Kim H.S., Choi D.Y., Yun S.J., Choi S.M., Kang J.W., Jung J.W., Hwang D., Kim K.P., Kim D.W. 2012. Proteomic analysis of microvesicles derived from human mesenchymal stem cells. J. Proteome Res. 11 (2), 839–849.CrossRefGoogle Scholar
  71. 71.
    Xie L., Mao M., Zhou L., Jiang B. 2016. Spheroid mesenchymal stem cells and mesenchymal stem cell-derived microvesicles: Two potential therapeutic strategies. Stem Cells Dev. 25 (3), 203–213.CrossRefGoogle Scholar
  72. 72.
    Zhou Y., Xu H., Xu W., Wang B., Wu H., Tao Y., Zhang B., Wang M., Mao F., Yan Y., Gao S., Gu H., Zhu W., Qian H. 2013. 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. 4 (2), 34.CrossRefGoogle Scholar
  73. 73.
    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. (Berl). 92 (4), 387–397.CrossRefGoogle Scholar
  74. 74.
    Zhang B., Yin Y., Lai R.C., Tan S.S., Choo A.B., Lim S.K. 2014. Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells Dev. 23 (11), 1233–1244.CrossRefGoogle Scholar
  75. 75.
    Zhu Y.G., Feng X.M., Abbott J. 2014. Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells. 32 (1), 116–125.CrossRefGoogle Scholar
  76. 76.
    Akyurekli C., Le Y., Richardson R.B., Fergusson D., Tay J., Allan D.S. 2015. A systematic review of preclinical studies on the therapeutic potential of mesenchymal stromal cell-derived microvesicles. Stem Cell Rev. 11 (1), 150–160.CrossRefGoogle Scholar
  77. 77.
    Zhang J., Guan J., Niu X., Hu G., Guo S., Li Q., Xie Z., Zhang C., Wang Y. 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.CrossRefGoogle Scholar
  78. 78.
    Zhang S., Chu W.C., Lai R.C., Lim S.K., Hui J.H., Toh W.S. 2016. Exosomes derived from human embryonic mesenchymal stem cells promote osteochondral regeneration. Osteoarthritis Cartilage. 24 (12), 2135–2140.CrossRefGoogle Scholar
  79. 79.
    Wen S., Dooner M., Cheng Y., Papa E., Del Tatto M., Pereira M., Deng Y., Goldberg L., Aliotta J., Chatterjee D., Stewart C., Carpanetto A., Collino F., Bruno S., Camussi G., Quesenberry P. 2016. Mesenchymal stromal cell-derived extracellular vesicles rescue radiation damage to murine marrow hematopoietic cells. Leukemia. 30 (11), 2221–2231.CrossRefGoogle Scholar
  80. 80.
    Li T., Yan Y., Wang B., Qian H., Zhang X., Shen L., Wang M., Zhou Y., Zhu W., Li W., Xu W. 2012. Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev. 22 (6), 845–854.CrossRefGoogle Scholar
  81. 81.
    Tan C.Y., Lai R.C., Wong W., Dan Y.Y., Lim S.K., Ho H.K. 2014. Mesenchymal stem cell-derived exosomes promote hepatic regeneration in drug-induced liver injury models. Stem Cell Res. Ther. 5 (3), 76.CrossRefGoogle Scholar
  82. 82.
    Collino F., Pomatto M., Bruno S., Lindoso R.S., Tapparo M., Sicheng W., Quesenberry P., Camussi G. 2017. Exosome and microvesicle-enriched fractions isolated from mesenchymal stem cells by gradient separation showed different molecular signatures and functions on renal tubular epithelial cells. Stem Cell Rev. 13 (2), 226–243.CrossRefGoogle Scholar
  83. 83.
    Aliotta J.M., Pereira M., Wen S., Dooner M.S., Del Tatto M., Papa E., Goldberg L.R., Baird G.L., Ventetuolo C.E., Quesenberry P.J., Klinger J.R. 2016. Exosomes induce and reverse monocrotaline-induced pulmonary hypertension in mice. Cardiovasc. Res. 110 (3), 319–330.CrossRefGoogle Scholar
  84. 84.
    Kang D., Oh S., Ahn S.M., Lee B.H., Moon M.H. 2008. Proteomic analysis of exosomes from human neural stem cells by flow field-flow fractionation and nanoflow liquid chromatography-tandem mass spectrometry. J. Proteome Res. 7 (8), 3475–3480.CrossRefGoogle Scholar
  85. 85.
    Bátiz L.F., Castro M.A., Burgos P.V., Velásquez Z.D., Muñoz R.I., Lafourcade C.A., Troncoso-Escudero P., Wyneken U. 2015. Exosomes as novel regulators of adult neurogenic niches. Front. Cell Neurosci. 9, 501.Google Scholar
  86. 86.
    Ratajczak J., Kucia M., Mierzejewska K., Marlicz W., Pietrzkowski Z., Wojakowski W., Greco N.J., Tendera M., Ratajczak M.Z. 2013. Paracrine proangiopoietic effects of human umbilical cord blood-derived purified CD133+ cells–implications for stem cell therapies in regenerative medicine. Stem Cells Dev. 22 (3), 422–430.CrossRefGoogle Scholar
  87. 87.
    Cantaluppi V., Gatti S., Medica D., Figliolini F., Bruno S., Deregibus M.C., Sordi A., Biancone L., Tetta C., Camussi G. 2012. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 82 (4), 412–427.CrossRefGoogle Scholar
  88. 88.
    Ranghino A., Cantaluppi V., Grange C., Vitillo L., Fop F., Biancone L., Deregibus M.C., Tetta C., Segoloni G.P., Camussi G. 2012. Endothelial progenitor cell-derived microvesicles improve neovascularization in a murine model of hindlimb ischemia. Int. J. Immunopathol. Pharmacol. 25 (1), 75–85.CrossRefGoogle Scholar
  89. 89.
    Chen L., Wang Y., Pan Y., Zhang L., Shen C., Qin G., Ashraf M., Weintraub N., Ma G., Tang Y. 2013. Cardiac progenitor-derived exosomes protect ischemic myocardium from acute ischemia/reperfusion injury. Biochem. Biophys. Res. Commun. 431 (3), 566–571.CrossRefGoogle Scholar
  90. 90.
    Herrera M. B., Fonsato V., Gatti S., Deregibus M.C., Sordi A., Cantarella D., Calogero R., Bussolati B., Tetta C., Camussi G. 2010. Human liver stem cell-derived microvesicles accelerate hepatic regeneration in hepatectomized rats. J. Cell. Mol. Med. 14 (6), 1605–1618.CrossRefGoogle Scholar
  91. 91.
    Kubikova I., Konecna H., Sedo O., Zdrahal Z., Rehulka P., Hribkova H., Rehulkova H., Hampl A., Chmelik J., Dvorak P. 2009. Proteomic profiling of human embryonic stem cell-derived microvesicles reveals a risk of transfer of proteins of bovine and mouse origin. Cytotherapy. 11 (3), 330–340.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • O. N. Sheveleva
    • 1
  • E. I. Domaratskaya
    • 1
  • O. V. Payushina
    • 1
    Email author
  1. 1.Koltzov Institute of Developmental Biology, Russian Academy of SciencesMoscowRussia

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