Abstract
In the past decade a number of different stem cell types have entered the clinical applications increasingly as a therapeutic option, due to their tissue maintenance capacity at the site where they localize. Although it was initially thought that conferral of resilience to damaged tissue largely depends on the stem cells themselves through orchestration of signaling among the local epithelial and immune systems at the injury site, recent findings point out that the remarkable regenerative capacity of stem cells is rather due to their nanovesicular products that emerge as the new active players of tissue repair processes. Among these extracellular vesicles exosomes generated particularly by stem cells have been receiving a substantial interest both in the fields of stem cell biology and extracellular vesicles. In this chapter fundamental facts about stem cell biology, biogenesis of extracellular vesicles and exosomes, their structure, and function are summarized. Moreover, properties of both tumor-derived exosomes as well as those derived from stem cells are discussed relatively in-depth in terms of their influence on proximal and distal tissue physiology. Last but not the least, among countless studies in an exploding field, we summarize those that attempt to unravel the complex signaling networks through which stem cell-derived exosomes alter the fate of differentiating stem cells as well as the molecular make-up of exosomes released from differentiating stem cells by conducting thorough proteomic and genomic analyses with the ultimate goal of identifying effector gene products mediating exosomal cues in stem cell biology.
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- Alix:
-
Apoptosis-linked gene 2–interacting protein X
- ASCs:
-
Adult Stem Cells
- BMSCs:
-
Bone marrow stem cells
- DCs:
-
Dendritic cells
- EGF:
-
Epidermal growth factor
- ESCs:
-
Embryonic stem cells
- EVs:
-
Extracellular vesicles
- HMSCs:
-
Human marrow stromal cells
- HSCs:
-
Hematopoietic Stem Cells
- HSP:
-
Heat-shock proteins
- ILVs:
-
Intraluminal vesicles
- iPSC:
-
Induced pluripotent stem cells
- MHC:
-
Major histocompatibility complex
- miRNA:
-
MicroRNA
- MSCs:
-
Mesenchymal stem cells
- MVB:
-
Multi-vesicular bodies
- Runx2:
-
Runt-related transcription factor 2
- TEX:
-
Tumor-derived exosomes
- TLR:
-
Toll-like receptors
References
Admyre C, Johansson SM, Qazi KR, Filén J-J, Lahesmaa R, Norman M, Neve EP, Scheynius A, Gabrielsson S (2007) Exosomes with immune modulatory features are present in human breast milk. J Immunol 179(3):1969–1978
Akyurekli C, Le Y, Richardson RB, Fergusson D, Tay J, Allan DS (2015) A systematic review of preclinical studies on the therapeutic potential of mesenchymal stromal cell-derived microvesicles. Stem Cell Rev Rep 11(1):150–160
Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29(4):341–345
Anderson JD, Johansson HJ, Graham CS, Vesterlund M, Pham MT, Bramlett CS, Montgomery EN, Mellema MS, Bardini RL, Contreras Z (2016) Comprehensive proteomic analysis of mesenchymal stem cell exosomes reveals modulation of angiogenesis via nuclear factor-kappaB signaling. Stem Cells 34(3):601–613
Bakhshandeh B, Amin Kamaleddin M, Aalishah K (2017) A comprehensive review on exosomes and microvesicles as epigenetic factors. Curr Stem Cell Res Ther 12(1):31–36
Bang C, Thum T (2012) Exosomes: new players in cell–cell communication. Int J Biochem Cell Biol 44(11):2060–2064
Behbahani GD, Khani S, Hosseini HM, Abbaszadeh-Goudarzi K, Nazeri S (2016) The role of exosomes contents on genetic and epigenetic alterations of recipient cancer cells. Iran J Basic Med Sci 19(10):1031–1039
Bobrie A, Colombo M, Raposo G, Théry C (2011) Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 12(12):1659–1668
Boon RA, Vickers KC (2013) Intercellular transport of microRNAs. Arterioscler Thromb Vasc Biol 33(2):186–192
Boyiadzis M, Whiteside TL (2015) Information transfer by exosomes: a new frontier in hematologic malignancies. Blood Rev 29(5):281–290
Caby M-P, Lankar D, Vincendeau-Scherrer C, Raposo G, Bonnerot C (2005) Exosomal-like vesicles are present in human blood plasma. Int Immunol 17(7):879–887
Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L (2010) Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 78(9):838–848
Chen TS, Lai RC, Lee MM, Choo ABH, Lee CN, Lim SK (2009) Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs. Nucleic Acids Res 38(1):215–224
Chin S-P, Poey AC, Wong C-Y, Chang S-K, Tan C-S, Ng M-T, Chew K-H, Lam K-H, Cheong S-K (2011) Intramyocardial and intracoronary autologous bone marrow-derived mesenchymal stromal cell treatment in chronic severe dilated cardiomyopathy. Cytotherapy 13(7):814–821
Choi H, Mun JY (2017) Structural analysis of exosomes using different types of Electron microscopy. Appl Microsc 47(3):171–175
Chowdhury R, Webber JP, Gurney M, Mason MD, Tabi Z, Clayton A (2015) Cancer exosomes trigger mesenchymal stem cell differentiation into pro-angiogenic and pro-invasive myofibroblasts. Oncotarget 6(2):715–731
Clayton A, Turkes A, Dewitt S, Steadman R, Mason MD, Hallett MB (2004) Adhesion and signaling by B cell-derived exosomes: the role of integrins. FASEB J 18(9):977–979
da Silva Meirelles L, Fontes AM, Covas DT, Caplan AI (2009) Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev 20(5):419–427
De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ (2007) Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25(1):100–106
DelaRosa O, Lombardo E (2010) Modulation of adult mesenchymal stem cells activity by toll-like receptors: implications on therapeutic potential. Mediat Inflamm 2010:1–9
Denzer K, van Eijk M, Kleijmeer MJ, Jakobson E, de Groot C, Geuze HJ (2000) Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J Immunol 165(3):1259–1265
Derkus B, Emregul KC, Emregul E (2017) A new approach in stem cell research—exosomes: their mechanism of action via cellular pathways. Cell Biol Int 41(5):466–475
Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315–317
Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo GJ (2012) MicroRNAs bind to toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci 109(31):E2110–E2116
Fatima F, Nawaz M (2015) Stem cell-derived exosomes: roles in stromal remodeling, tumor progression, and cancer immunotherapy. Chin J Cancer 34(3):46
Franceschi RT, Ge C, Xiao G, Roca H, Jiang D (2007) Transcriptional regulation of osteoblasts. Ann N Y Acad Sci 1116(1):196–207
Friedenstein A, Chailakhjan R, Lalykina K (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Prolif 3(4):393–403
Ge M, Ke R, Cai T, Yang J, Mu X (2015) Identification and proteomic analysis of osteoblast-derived exosomes. Biochem Biophys Res Commun 467(1):27–32
Ghannam S, Bouffi C, Djouad F, Jorgensen C, Noël D (2010) Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications. Stem Cell Res Ther 1(1):2
Giobbe GG, Michielin F, Luni C, Giulitti S, Martewicz S, Dupont S, Floreani A, Elvassore N (2015) Functional differentiation of human pluripotent stem cells on a chip. Nat Methods 12(7):637–640
Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci 97(25):13625–13630
Hao S, Ye Z, Li F, Meng Q, Qureshi M, Yang J, Xiang J (2006) Epigenetic transfer of metastatic activity by uptake of highly metastatic B16 melanoma cell-released exosomes. Exp Oncol 28(2):126–131
Hao ZC, Lu J, Wang SZ, Wu H, Zhang YT, Xu SG (2017) Stem cell-derived exosomes: a promising strategy for fracture healing. Cell Prolif 50(5):e12359
Henningson CT Jr, Stanislaus MA, Gewirtz AM (2003) 28. Embryonic and adult stem cell therapy. J Allergy Clin Immunol 111(2):S745–S753
Higuchi A, Ling Q-D, Ko Y-A, Chang Y, Umezawa A (2011) Biomaterials for the feeder-free culture of human embryonic stem cells and induced pluripotent stem cells. Chem Rev 111(5):3021–3035
Hood JL, San RS, Wickline SA (2011) Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 71(11):3792–3801
Jiang J, Lv Z, Gu Y, Li J, Xu L, Xu W, Lu J, Xu J (2010) Adult rat mesenchymal stem cells differentiate into neuronal-like phenotype and express a variety of neuro-regulatory molecules in vitro. Neurosci Res 66(1):46–52
Johnstone RM, Adam M, Hammond J, 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
Kalluri R (2016) The biology and function of exosomes in cancer. J Clin Invest 126(4):1208–1215
Kamerkar S, LeBleu VS, Sugimoto H, Yang S, Ruivo CF, Melo SA, Lee JJ, Kalluri R (2017) Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature 546(7659):498–503
Karin M, Mintz B (1981) Receptor-mediated endocytosis of transferrin in developmentally totipotent mouse teratocarcinoma stem cells. J Biol Chem 256(7):3245–3252
Keshtkar S, Azarpira N, Ghahremani MH (2018) Mesenchymal stem cell-derived extracellular vesicles: novel frontiers in regenerative medicine. Stem Cell Res Ther 9(1):63
Komori T (2006) Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 99(5):1233–1239
Konala VBR, Mamidi MK, Bhonde R, Das AK, Pochampally R, Pal R (2016) The current landscape of the mesenchymal stromal cell secretome: a new paradigm for cell-free regeneration. Cytotherapy 18(1):13–24
Lai RC, Arslan F, Lee MM, Sze NSK, Choo A, Chen TS, Salto-Tellez M, Timmers L, Lee CN, El Oakley RM (2010) Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 4(3):214–222
Lai RC, Chen TS, Lim SK (2011) Mesenchymal stem cell exosome: a novel stem cell-based therapy for cardiovascular disease. Regen Med 6(4):481–492
Lai RC, Tan SS, Teh BJ, Sze SK, Arslan F, De Kleijn DP, Choo A, Lim SK (2012) Proteolytic potential of the MSC exosome proteome: implications for an exosome-mediated delivery of therapeutic proteasome. Int J Proteomics 2012:1–14
Lai RC, Yeo RWY, Tan KH, Lim SK (2013a) Exosomes for drug delivery—a novel application for the mesenchymal stem cell. Biotechnol Adv 31(5):543–551
Lai RC, Yeo RWY, Tan SS, Zhang B, Yin Y, Sze NSK, Choo A, Lim SK (2013b) Mesenchymal stem cell exosomes: the future MSC-based therapy? Mesenchymal stem cell therapy. Humana Press, Totowa, NJ, pp 39–61
Lai RC, Yeo RWY, Lim SK (2015) Mesenchymal stem cell exosomes. Semin Cell Dev Biol 40:82–88. Elsevier
Laude AJ, Prior IA (2004) Plasma membrane microdomains: organization, function and trafficking. Mol Membr Biol 21(3):193–205
Laulagnier K, Motta C, Hamdi S, Sébastien R, Fauvelle F, Pageaux J-F, Kobayashi T, Salles J-P, Perret B, Bonnerot C (2004) Mast cell-and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J 380(1):161–171
Le MT, Xie H, Zhou B, Chia PH, Rizk P, Um M, Udolph G, Yang H, Lim B, Lodish HF (2009) MicroRNA-125b promotes neuronal differentiation in human cells by repressing multiple targets. Mol Cell Biol 29(19):5290–5305
Li Z, Margariti A, Wu Y, Yang F, Hu J, Zhang L, Chen T (2015) MicroRNA-199a induces differentiation of induced pluripotent stem cells into endothelial cells by targeting sirtuin 1. Mol Med Rep 12(3):3711–3717
Ludwig S, Floros T, Theodoraki M-N, Hong C-S, Jackson EK, Lang S, Whiteside TL (2017) Suppression of lymphocyte functions by plasma exosomes correlates with disease activity in patients with head and neck cancer. Clin Cancer Res 23(16):4843–4854. https://doi.org/10.1158/1078-0432.CCR-16-2819
Mareschi K, Biasin E, Piacibello W, Aglietta M, Madon E, Fagioli F (2001) Isolation of human mesenchymal stem cells: bone marrow versus umbilical cord blood. Haematologica 86(10):1099–1100
Miao Z, Jin J, Chen L, Zhu J, Huang W, Zhao J, Qian H, Zhang X (2006) Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int 30(9):681–687
Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ, Bernad A, Sánchez-Madrid F (2011) Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2:282
Möbius W, Ohno-Iwashita Y, EGV D, Oorschot VM, Shimada Y, Fujimoto T, Heijnen HF, Geuze HJ, Slot JW (2002) Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. J Histochem Cytochem 50(1):43–55
Morsczeck C, Götz W, Schierholz J, Zeilhofer F, Kühn U, Möhl C, Sippel C, Hoffmann K (2005) Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24(2):155–165
Narayanan R, Huang C-C, Ravindran S (2016) Hijacking the cellular mail: exosome mediated differentiation of mesenchymal stem cells. Stem Cells Int 2016:1–11
Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448(7151):313
Pan B-T, Johnstone RM (1983) Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33(3):967–978
Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Würdinger T, Middeldorp JM (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci 107(14):6328–6333
Pfister O, Della Verde G, Liao R, Kuster GM (2014) Regenerative therapy for cardiovascular disease. Transl Res 163(4):307–320
Phinney DG, Prockop DJ (2007) Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—current views. Stem Cells 25(11):2896–2902
Qi X, Zhang J, Yuan H, Xu Z, Li Q, Niu X, Hu B, Wang Y, Li X (2016) Exosomes secreted by human-induced pluripotent stem cell-derived mesenchymal stem cells repair critical-sized bone defects through enhanced angiogenesis and osteogenesis in osteoporotic rats. Int J Biol Sci 12(7):836–849
Rabinowits G, Gerçel-Taylor C, Day JM, Taylor DD, Kloecker GH (2009) Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer 10(1):42–46
Rajendran L, Simons K (2005) Lipid rafts and membrane dynamics. J Cell Sci 118(6):1099–1102
Rani S, Ryan AE, Griffin MD, Ritter T (2015) Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther 23(5):812–823
Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200(4):373–383
Ratajczak MZ, Ciechanowicz AK, Kucharska-Mazur J, Samochowiec J (2017) Stem cells and their potential clinical applications in psychiatric disorders. Prog Neuro-Psychopharmacol Biol Psychiatry 80(Pt A):3–9
Schorey JS, Bhatnagar S (2008) Exosome function: from tumor immunology to pathogen biology. Traffic 9(6):871–881
Schuldiner M, Yanuka O, Itskovitz-Eldor J, Melton DA, Benvenisty N (2000) Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci 97(21):11307–11312
Simpson RJ, Jensen SS, Lim JW (2008) Proteomic profiling of exosomes: current perspectives. Proteomics 8(19):4083–4099
Skog J, Würdinger T, Van Rijn S, Meijer DH, Gainche L, 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(12):1470–1476
Suzuki N, Shimizu J, Takai K, Arimitsu N, Ueda Y, Takada E, Hirotsu C, Suzuki T, Fujiwara N, Tadokoro M (2012) Establishment of retinal progenitor cell clones by transfection with Pax6 gene of mouse induced pluripotent stem (iPS) cells. Neurosci Lett 509(2):116–120
Szczepanski MJ, Szajnik M, Welsh A, Whiteside TL, Boyiadzis M (2011) Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-β1. Haematologica 96(9):1302–1309
Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676
Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872
Takeda YS, Xu Q (2015) Neuronal differentiation of human mesenchymal stem cells using exosomes derived from differentiating neuronal cells. PLoS One 10(8):e0135111
Taylor DD, Gercel-Taylor C (2008) MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 110(1):13–21
Théry C, Regnault A, Garin J, Wolfers J, Zitvogel L, Ricciardi-Castagnoli P, Raposo G, Amigorena S (1999) Molecular characterization of dendritic cell-derived exosomes: selective accumulation of the heat shock protein hsc73. J Cell Biol 147(3):599–610
Théry C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2(8):569–579
Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147
Tsao C-R, Liao M-F, Wang M-h, Cheng C-M, Chen C-H (2014) Mesenchymal stem cell derived exosomes: a new hope for the treatment of cardiovascular disease? Acta Cardiol Sin 30(5):395–400
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9(6):654–659
Van der Pol E, Böing AN, Harrison P, Sturk A, Nieuwland R (2012) Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev 64(3):676–705
Vlassov AV, Magdaleno S, Setterquist R, Conrad R (2012) Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta 1820(7):940–948
Whiteside T (2017) Exosomes carrying immunoinhibitory proteins and their role in cancer. Clin Exp Immunol 189(3):259–267
Whiteside TL (2018) Exosome and mesenchymal stem cell cross-talk in the tumor microenvironment. Semin Immunol 35:69–79. Elsevier
Wilson A, Trumpp A (2006) Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 6(2):93–106
Witkowska-Zimny M, Walenko K (2011) Stem cells from adipose tissue. Cell Mol Biol Lett 16(2):236–257
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 (2014) Altered microRNA expression profile in exosomes during osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. PLoS One 9(12):e114627
Xu J, Liao K, Zhou W (2018) Exosomes regulate the transformation of cancer cells in cancer stem cell homeostasis. Stem Cells Int 2018:1–16
Yalvaç ME, Yilmaz A, Mercan D, Aydin S, Dogan A, Arslan A, Demir Z, Salafutdinov II, Shafigullina AK, Sahin F (2011) Differentiation and neuro-protective properties of immortalized human tooth germ stem cells. Neurochem Res 36(12):2227–2235
Yamashita YM, Jones DL, Fuller MT (2003) Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 301(5639):1547–1550
Young HE, Steele TA, Bray RA, Hudson J, Floyd JA, Hawkins K, Thomas K, Austin T, Edwards C, Cuzzourt J (2001) Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat Rec 264(1):51–62
Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920
Yu B, Zhou S, Wang Y, Qian T, Ding G, Ding F, Gu X (2012) miR-221/222 promote Schwann cell proliferation and migration by targeting LASS2 following sciatic nerve injury. J Cell Sci 125(Pt 11):2675–2683. https://doi.org/10.1242/jcs.098996
Yu B, Zhang X, Li X (2014) Exosomes derived from mesenchymal stem cells. Int J Mol Sci 15(3):4142–4157
Yuan Z, Kolluri KK, Gowers KH, Janes SM (2017) TRAIL delivery by MSC-derived extracellular vesicles is an effective anticancer therapy. J Extracell Vesicles 6(1):1265291
Zhang W-B, Zhong W-J, Wang L (2014) A signal-amplification circuit between miR-218 and Wnt/β-catenin signal promotes human adipose tissue-derived stem cells osteogenic differentiation. Bone 58:59–66
Zhang J, Liu X, Li H, Chen C, Hu B, Niu X, Li Q, Zhao B, Xie Z, Wang Y (2016) Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway. Stem Cell Res Ther 7(1):136
Zheng G, Huang R, Qiu G, Ge M, Wang J, Shu Q, Xu J (2018) Mesenchymal stromal cell-derived extracellular vesicles: regenerative and immunomodulatory effects and potential applications in sepsis. Cell Tissue Res 374(1):1–15
Zhou H, Pisitkun T, Aponte A, Yuen PS, Hoffert JD, Yasuda H, Hu X, Chawla L, Shen R-F, Knepper MA (2006) Exosomal Fetuin-A identified by proteomics: a novel urinary biomarker for detecting acute kidney injury. Kidney Int 70(10):1847–1857
Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, Oeh J, Modrusan Z, Bais C, Sampath D (2012) Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J 31(17):3513–3523
Zomer A, Vendrig T, Hopmans ES, van Eijndhoven M, Middeldorp JM, Pegtel DM (2010) Exosomes: fit to deliver small RNA. Commun Integr Biol 3(5):447–450
Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7(2):211–228
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Abdik, H., Avsar Abdik, E., Hızlı Deniz, A.A., Taşlı, P.N., Şahin, F. (2019). A Novel Virtue in Stem Cell Research: Exosomes and Their Role in Differentiation. In: Turksen, K. (eds) Cell Biology and Translational Medicine, Volume 5. Advances in Experimental Medicine and Biology(), vol 1144. Springer, Cham. https://doi.org/10.1007/5584_2019_339
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