REVIEW

The mini player with diverse functions: extracellular vesicles in cell biology, disease, and therapeutics

  • Abhimanyu Thakur 1,2 ,
  • Xiaoshan Ke 1,2 ,
  • Ya-Wen Chen 3,4 ,
  • Pedram Motallebnejad 1,2 ,
  • Kui Zhang 1,2 ,
  • Qizhou Lian , 5,6,7 ,
  • Huanhuan Joyce Chen , 1,2
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  • 1. The Pritzker School of Molecular Engineering, The University of Chicago, Chicago, Illinois, USA
  • 2. The Ben May Department for Cancer Research, The University of Chicago, Chicago, Illinois, USA
  • 3. Division of Pulmonary, Critical Care and Sleep Medicine, Department of Medicine, Keck School of Medicine, Hastings Center for Pulmonary Research, University of Southern California, Los Angeles, CA 90089, USA
  • 4. Department of Stem Cell Biology and Regenerative Biology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90089, USA
  • 5. Department of Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pok Fu Lam, Hong Kong, China
  • 6. Prenatal Diagnostic Center and Cord Blood Bank, Guangzhou Women and Children’s Medical Center, Guangzhou Medical University, Guangzhou, China
  • 7. HKUMed Laboratory of Cellular Therapeutics, the University of Hong Kong, Pok Fu Lam, Hong Kong, China
qzlian@hku.hk (Q. Lian)
joycechen@uchicago.edu (H. J. Chen)

Received date: 06 May 2021

Accepted date: 08 Jul 2021

Published date: 15 Sep 2022

Copyright

2021 The Author(s)

Abstract

Extracellular vesicles (EVs) are tiny biological nanovesicles ranging from approximately 30–1000 nm in diameter that are released into the extracellular matrix of most cell types and in biofluids. The classification of EVs includes exosomes, microvesicles, and apoptotic bodies, dependent on various factors such as size, markers, and biogenesis pathways. The transition of EV relevance from that of being assumed as a trash bag to be a key player in critical physiological and pathological conditions has been revolutionary in many ways. EVs have been recently revealed to play a crucial role in stem cell biology and cancer progression via intercellular communication, contributing to organ development and the progression of cancer. This review focuses on the significant research progress made so far in the role of the crosstalk between EVs and stem cells and their niche, and cellular communication among different germ layers in developmental biology. In addition, it discusses the role of EVs in cancer progression and their application as therapeutic agents or drug delivery vehicles. All such discoveries have been facilitated by tremendous technological advancements in EV-associated research, especially the microfluidics systems. Their pros and cons in the context of characterization of EVs are also extensively discussed in this review. This review also deliberates the role of EVs in normal cell processes and disease conditions, and their application as a diagnostic and therapeutic tool. Finally, we propose future perspectives for EV-related research in stem cell and cancer biology.

Cite this article

Abhimanyu Thakur , Xiaoshan Ke , Ya-Wen Chen , Pedram Motallebnejad , Kui Zhang , Qizhou Lian , Huanhuan Joyce Chen . The mini player with diverse functions: extracellular vesicles in cell biology, disease, and therapeutics[J]. Protein & Cell, 2022 , 13(9) : 631 -654 . DOI: 10.1007/s13238-021-00863-6

1
Alberti C, Cochella L(2017) A framework for understanding the roles of miRNAs in animal development. Development 144:2548–2559

DOI

2
Aliotta JM, Pereira M, Johnson KW(2010) Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription. Exp Hematol 38:233–245

DOI

3
Anderson RL, Balasas T, Callaghan J(2019) A framework for the development of effective anti-metastatic agents. Nat Rev Clin Oncol 16:185–204

DOI

4
André F, Chaput N, Schartz NEC(2004) Exosomes as Potent Cell-Free Peptide-Based Vaccine. I. Dendritic Cell-Derived Exosomes Transfer Functional MHC Class I/Peptide Complexes to Dendritic Cells. J Immunol 172:2126–2136

DOI

5
Arslan F, Lai RC, Smeets MB (2013) Mesenchymal stem cellderived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res 10:301–312

DOI

6
Aryani A, Denecke B(2016) Exosomes as a Nanodelivery system: a key to the future of neuromedicine? Mol Neurobiol 53:818–834

DOI

7
Asea A, Jean-Pierre C, Kaur P(2008) Heat shock proteincontaining exosomes in mid-trimester amniotic fluids. J Reprod Immunol 79:12–17

DOI

8
Baquir B, Hancock REW(2017) Exosomes, your body’s answer to immune health. Ann Transl Med 5:81–81

DOI

9
Baskar R, Lee KA, Yeo R, Yeoh K-W(2012) Cancer and radiation therapy: current advances and future directions. Int J Med Sci 9:193–199

DOI

10
Basu B, Ghosh MK(2019) Extracellular vesicles in glioma: from diagnosis to therapy. BioEssays 41:1800245

DOI

11
Battaglia R, Palini S, Vento ME(2019) Identification of extracellular vesicles and characterization of miRNA expression profiles in human blastocoel fluid. Sci Rep 9:84

DOI

12
Becker JC(2014) Tumor-educated myeloid cells: impact the microand macroenvironment. Exp Dermatol 23:157–158

DOI

13
Beer KB, Wehman AM(2017) Mechanisms and functions of extracellular vesicle release in vivo—what we can learn from flies and worms. Cell Adh Migr 11:135–150

DOI

14
Bellavia D, Raimondi L, Costa V(2018) Engineered exosomes: a new promise for the management of musculoskeletal diseases. Biochim Biophys Acta 1862:1893–1901

DOI

15
Benedikter BJ, Bouwman FG, Vajen T(2017) Ultrafiltration combined with size exclusion chromatography efficiently isolates extracellular vesicles from cell culture media for compositional and functional studies. Sci Rep 7:15297

DOI

16
Bernard V, Ling J, Maitra A(2018) Heterogeneity of tumor exosomes –role in precision medicine. In: Diagnostic and therapeutic applications of exosomes in cancer. Elsevier, Amsterdam,pp 59–67

DOI

17
Bier E, De Robertis EM(2015) BMP gradients: a paradigm for morphogen-mediated developmental patterning. Science 348: aaa5838–aaa5838

DOI

18
Böing AN, van der Pol E, Grootemaat AE(2014) Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles 3:23430

DOI

19
Booth AM, Fang Y, Fallon JK (2006) Exosomes and HIV gag bud from endosome-like domains of the Tcell plasma membrane. J Cell Biol 172:923–935

DOI

20
Boriachek K, Islam MN, Gopalan V (2017) Quantum dot-based sensitive detection of disease specific exosome in serum. Analyst 142:2211–2219

DOI

21
Budnik V, Ruiz-Cañada C, Wendler F(2016) Extracellular vesicles round off communication in the nervous system. Nat Rev Neurosci 17:160–172

DOI

22
Bunggulawa EJ, Wang W, Yin T (2018) Recent advancements in the use of exosomes as drug delivery systems. J Nanobiotechnol 16:81

DOI

23
Camussi G, Deregibus MC, Bruno S (2010) Exosomes/ microvesicles as a mechanism of cell-to-cell communication. Kidney Int 78:838–848

DOI

24
Cao M, Ning J, Hernandez-Lara CI (2015) Uni-directional ciliary membrane protein trafficking by a cytoplasmic retrograde IFT motor and ciliary ectosome shedding. Elife. https://doi.org/10. 7554/eLife.05242

DOI

25
Cappello V, Marchetti L, Parlanti P (2016) Ultrastructural characterization of the lower motor system in a mouse model of Krabbe disease. Sci Rep 6:1

DOI

26
Carmicheal J, Hayashi C, Huang X (2019) Label-free characterization of exosome via surface enhanced Raman spectroscopy for the early detection of pancreatic cancer. Nanomed Nanotechnol Biol Med 16:88–96

DOI

27
Chaffer CL, Weinberg RA(2011) A perspective on cancer cell metastasis. Science 331:1559–1564

DOI

28
Chalmin F, Ladoire S, Mignot G (2010) Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloidderived suppressor cells. J Clin Invest. https://doi.org/10.1172/ JCI40483

29
Chang JC(2016) Cancer stem cells. Medicine (baltimore) 95:S20–S25

DOI

30
Chen I-H, Xue L, Hsu C-C(2017a) Phosphoproteins in extracellular vesicles as candidate markers for breast cancer. Proc Natl Acad Sci 114:3175–3180

DOI

31
Chen Z, Li Y, Yu H, (2017b) Isolation of extracellular vesicles from stem cells. pp 389–394

DOI

32
Chernyshev VS, Rachamadugu R, Tseng YH(2015) Size and shape characterization of hydrated and desiccated exosomes. Anal Bioanal Chem 407:3285–3301

DOI

33
Cho S, Jo W, Heo Y (2016) Isolation of extracellular vesicle from blood plasma using electrophoretic migration through porous membrane. Sens Actuators B Chem 233:289–297

DOI

34
Choi H, Mun JY(2017) Structural analysis of exosomes using different types of electron microscopy. Appl Microsc 47:171–175

DOI

35
Colombo M, Raposo G, Théry C(2014) Biogenesis, secretion, and iIntercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 30:255–289

DOI

36
Conde-Vancells J, Rodriguez-Suarez E, Embade N (2008) Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J Proteome Res 7:5157–5166

DOI

37
Contreras-Naranjo JC, Wu H-J, Ugaz VM(2017) Microfluidics for exosome isolation and analysis: enabling liquid biopsy for personalized medicine. Lab Chip 17:3558–3577

DOI

38
Corrado C, Raimondo S, Chiesi A (2013) Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications. Int J Mol Sci 14:5338–5366

DOI

39
Corrigan L, Redhai S, Leiblich A (2014) BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior. J Cell Biol 206:671–688

DOI

40
Costa-Silva B, Aiello NM, Ocean AJ (2015) Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol 17:816–826

DOI

41
Cruz L, Arevalo Romero JA, Brandão Prado M(2018a) Evidence of extracellular vesicles biogenesis and release in mouse embryonic stem cells. Stem Cell Rev Reports 14:262–276

DOI

42
Cruz L, Romero JAA, Iglesia RP, Lopes MH(2018b) Extracellular vesicles: decoding a new language for cellular communication in early embryonic development. Front Cell Dev Biol. https://doi.org/ 10.3389/fcell.2018.00094

DOI

43
Danilchik M, Williams M, Brown E(2013) Blastocoel-spanning filopodia in cleavage-stage Xenopus laevis: Potential roles in morphogen distribution and detection. Dev Biol 382:70–81

DOI

44
Davies RT, Kim J, Jang SC(2012) Microfluidic filtration system to isolate extracellular vesicles from blood. Lab Chip 12:5202

DOI

45
de la Gomez C T, Goreham RV, Bech Serra JJ (2018) “Exosomics”—a review of biophysics, biology and biochemistry of exosomes with a focus on human breast milk. Front Genet. https://doi.org/10.3389/fgene.2018.00092

DOI

46
de Menezes-Neto A, Sáez MJF, Lozano-Ramos I(2015) Sizeexclusion chromatography as a stand-alone methodology identifies novel markers in mass spectrometry analyses of plasmaderived vesicles from healthy individuals. J Extracell Vesicles 4:27378

DOI

47
De Toro J, Herschlik L, Waldner C, Mongini C(2015) Emerging roles of exosomes in normal and pathological conditions: new insights for diagnosis and therapeutic applications. Front Immunol. https:// doi.org/10.3389/fimmu.2015.00203

DOI

48
Deng T, Zhang H, Yang H(2020) Exosome miR-155 derived from gastric carcinoma promotes angiogenesis by targeting the c-MYB/VEGF axis of endothelial cells. Mol Ther Nucleic Acids 19:1449–1459

DOI

49
Deregibus MC, Cantaluppi V, Calogero R(2007) Endothelial progenitor cell–derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110:2440–2448

DOI

50
Desrochers LM, Bordeleau F, Reinhart-King CA(2016) Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat Commun 7:11958

DOI

51
Dignat-George F, Boulanger CM(2011) The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31:27–33

DOI

52
Dimov N, Kastner E, Hussain M (2017) Formation and purification of tailored liposomes for drug delivery using a module-based micro continuous-flow system. Sci Rep 7:12045

DOI

53
Draening T, Heigwer J, Juergensen L(2018) Extracellular vesicle-delivered bone morphogenetic proteins: a novel paracrine mechanism during embryonic development. BioRxiv. https://doi. org/10.1101/321356

DOI

54
Dudani JS, Gossett DR, Tse HTK(2015) Rapid inertial solution exchange for enrichment and flow cytometric detection of microvesicles. Biomicrofluidics 9:014112

DOI

55
Fairchild CL, Barna M(2014) Specialized filopodia: at the ‘tip’ of morphogen transport and vertebrate tissue patterning. Curr Opin Genet Dev 27:67–73

DOI

56
Fang S, Tian H, Li X(2017) Clinical application of a microfluidic chip for immunocapture and quantification of circulating exosomes to assist breast cancer diagnosis and molecular classification. PLoS ONE 12:e0175050

DOI

57
Filipe V, Hawe A, Jiskoot W(2010) Critical evaluation of nanoparticle tracking analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates. Pharm Res 27:796–810

DOI

58
Fröhlich D, Kuo WP, Frühbeis C(2014) Multifaceted effects of oligodendroglial exosomes on neurons: impact on neuronal firing rate, signal transduction and gene regulation. Philos Trans R Soc B Biol Sci 369:20130510

DOI

59
Frühbeis C, Fröhlich D, Kuo WP (2013) Neurotransmittertriggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol 11:e1001604

DOI

60
Gallagher S, Winston SE, Fuller SA, Hurrell JGR(2008) Immunoblotting and immunodetection. Curr Protoc Mol Biol. https://doi.org/10.1002/0471142727.mb1008s83

DOI

61
Gatti J-L, Métayer S, Belghazi M(2005) Identification, proteomic profiling, and origin of ram epididymal fluid exosomelike vesicles1. Biol Reprod 72:1452–1465

DOI

62
Goreham RV, Ayed Z, Amin ZM, Dobhal G(2020) The future of quantum dot fluorescent labelling of extracellular vesicles for biomedical applications. Nano Futur 4:022001

DOI

63
Gradilla A-C, González E, Seijo I (2014) Exosomes as Hedgehog carriers in cytoneme-mediated transport and secretion. Nat Commun 5:5649

DOI

64
Greco V, Hannus M, Eaton S(2001) Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 106:633–645

DOI

65
Gross JC, Chaudhary V, Bartscherer K, Boutros M(2012) Active Wnt proteins are secreted on exosomes. Nat Cell Biol 14:1036–1045

DOI

66
Gross N, Kropp J, Khatib H(2017) MicroRNA signaling in embryo development. Biology (basel) 6:34

DOI

67
Gualerzi A, Kooijmans SAA, Niada S (2019) Raman spectroscopy as a quick tool to assess purity of extracellular vesicle preparations and predict their functionality. J Extracell Vesicles 8:1568780

DOI

68
Gupta S, Knowlton AA(2007) HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway. Am J Physiol Circ Physiol 292:H3052–H3056

DOI

69
György B, Sage C, Indzhykulian AA (2017) Rescue of hearing by gene delivery to inner-ear hair cells using exosome-associated AAV. Mol Ther 25:379–391

DOI

70
Ha D, Yang N, Nadithe V(2016) Exosomes as therapeutic drug carriers and delivery vehicles across biological membranes: current perspectives and future challenges. Acta Pharm Sin B 6:287–296

DOI

71
Hardij J, Cecchet F, Berquand A(2013) Characterisation of tissue factor-bearing extracellular vesicles with AFM: comparison of air-tapping-mode AFM and liquid Peak Force AFM. J Extracell Vesicles 2:21045

DOI

72
Harding C, Heuser J, Stahl P(1984) Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: demonstration of a pathway for receptor shedding. Eur J Cell Biol 35:256–263

73
He L, Zhu W, Chen Q (2019) Ovarian cancer cell-secreted exosomal miR-205 promotes metastasis by inducing angiogenesis. Theranostics 9:8206–8220

DOI

74
He M, Crow J, Roth M (2014) Integrated immunoisolation and protein analysis of circulating exosomes using microfluidic technology. Lab Chip 14:3773

DOI

75
Heckman CA, Plummer HK(2013) Filopodia as sensors. Cell Signal 25:2298–2311

DOI

76
Hosseinkhani B, van den Akker N, D’Haen J(2017) Direct detection of nano-scale extracellular vesicles derived from inflammation-triggered endothelial cells using surface plasmon resonance. Nanomed Nanotechnol Biol Med 13:1663–1671

DOI

77
Hsu H-J, Bahader M, Lai C-M(2019) Molecular control of the female germline stem cell niche size in Drosophila. Cell Mol Life Sci 76:4309–4317

DOI

78
Huang H, Wang C, Liu F (2018) Reciprocal network between cancer stem-like cells and macrophages facilitates the progression and androgen deprivation therapy resistance of prostate cancer. Clin Cancer Res 24:4612–4626

DOI

79
Hur YH, Cerione RA, Antonyak MA(2020) Extracellular vesicles and their roles in stem cell biology. Stem Cells 38:469–476

DOI

80
Ibrahim AG-E, Cheng K, Marbán E(2014) Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Rep 2:606–619

DOI

81
Im H, Shao H, Il PY(2014) Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor. Nat Biotechnol 32:490–495

DOI

82
Im H, Yang K, Lee H, Castro CM(2017) Characterization of extracellular vesicles by surface plasmon resonance. pp 133–141

DOI

83
Jeong S, Park J, Pathania D (2016) Integrated magnetoelectrochemical sensor for exosome analysis. ACS Nano 10:1802–1809

DOI

84
Jiang D, Gao F, Zhang Y(2016) Mitochondrial transfer of mesenchymal stem cells effectively protects corneal epithelial cells from mitochondrial damage. Cell Death Dis 7:e2467–e2467

DOI

85
Jiang D, Xiong G, Feng H (2019) Donation of mitochondria by iPSC-derived mesenchymal stem cells protects retinal ganglion cells against mitochondrial complex I defect-induced degeneration. Theranostics 9:2395–2410

DOI

86
Jiang X-C, Gao J-Q(2017) Exosomes as novel bio-carriers for gene and drug delivery. Int J Pharm 521:167–175

DOI

87
Johnstone RM, Adam M, Hammond JR (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262:9412–9420

DOI

88
Jones DL, Wagers AJ(2008) No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 9:11–21

DOI

89
Jung YJ, Kim HK, Cho Y, (2020) Cell reprogramming using extracellular vesicles from differentiating stem cells into white/ beige adipocytes. Sci Adv 6:eaay6721

DOI

90
Kalluri R, LeBleu VS(2020) The biology, function , and biomedical applications of exosomes. Science 367:eaau6977

DOI

91
Kamerkar S, LeBleu VS, Sugimoto H(2017) Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature 546:498–503

DOI

92
Kanellopoulou C, Gilpatrick T, Kilaru G (2015) Reprogramming of polycomb-mediated gene silencing in embryonic stem cells by the miR-290 family and the methyltransferase Ash1l. Stem Cell Rep 5:971–978

DOI

93
Kanwar SS, Dunlay CJ, Simeone DM, Nagrath S(2014) Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip 14:1891–1900

DOI

94
Kao Y-C, Ho P-C, Tu Y-K (2020) Lipids and Alzheimer’s disease. Int J Mol Sci 21:1505

DOI

95
Kato S, Goodman A, Walavalkar V(2017) Hyperprogressors after immunotherapy: analysis of genomic alterations associated with accelerated growth rate. Clin Cancer Res 23:4242–4250

DOI

96
Kawakami K, Fujita Y, Matsuda Y(2017) Gamma-glutamyltransferase activity in exosomes as a potential marker for prostate cancer. BMC Cancer 17:316

DOI

97
Khan M, Nickoloff E, Abramova T (2015) Embryonic stem cellderived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ Res 117:52–64

DOI

98
Khawar MB, Abbasi MH, Siddique Z (2019) An update on novel therapeutic warfronts of extracellular vesicles (EVs) in cancer treatment: where we are standing right now and where to go in the future. Oxid Med Cell Longev 2019:1–21

DOI

99
Kim MS, Haney MJ, Zhao Y (2018) Engineering macrophagederived exosomes for targeted paclitaxel delivery to pulmonary metastases: in vitro and in vivo evaluations. Nanomed Nanotechnol Biol Med 14:195–204

DOI

100
Kirkeby A, Perlmann T, Pereira C-F(2016) The stem cell niche finds its true north. Development 143:2877–2881

DOI

101
Klinov D, Magonov S(2004) True molecular resolution in tappingmode atomic force microscopy with high-resolution probes. Appl Phys Lett 84:2697–2699

DOI

102
Ko J, Carpenter E, Issadore D(2016) Detection and isolation of circulating exosomes and microvesicles for cancer monitoring and diagnostics using micro-/nano-based devices. Analyst 141:450–460

DOI

103
Ko SY, Lee W, Kenny HA (2019) Cancer-derived small extracellular vesicles promote angiogenesis by heparin-bound, bevacizumab-insensitive VEGF, independent of vesicle uptake. Commun Biol 2:386

DOI

104
Koles K, Nunnari J, Korkut C(2012) Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J Biol Chem 287:16820–16834

DOI

105
Koritzinsky EH, Street JM, Star RA, Yuen PST(2017) Quantification of exosomes. J Cell Physiol 232:1587–1590

DOI

106
Korkut C, Ataman B, Ramachandran P (2009) Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell 139:393–404

DOI

107
Kwizera EA, O’Connor R, Vinduska V(2018) Molecular detection and analysis of exosomes using surface-enhanced Raman scattering gold nanorods and a miniaturized device. Theranostics 8:2722–2738

DOI

108
Lane RE, Korbie D, Hill MM, Trau M(2018) Extracellular vesicles as circulating cancer biomarkers: opportunities and challenges. Clin Transl Med 7:14

DOI

109
Le Borgne R, Schweisguth F(2003) Notch signaling: endocytosis makes delta signal better. Curr Biol 13:R273–R275

DOI

110
Lee K, Shao H, Weissleder R, Lee H(2015) Acoustic purification of extracellular microvesicles. ACS Nano 9:2321–2327

DOI

111
Li J, Chen Y, Guo X(2017) GPC1 exosome and its regulatory miRNAs are specific markers for the detection and target therapy of colorectal cancer. J Cell Mol Med 21:838–847

DOI

112
Li J, Sherman-Baust CA, Tsai-Turton M(2009) Claudincontaining exosomes in the peripheral circulation of women with ovarian cancer. BMC Cancer 9:244

DOI

113
Li L, Xie T(2005) STEM CELL NICHE: structure and function. Annu Rev Cell Dev Biol 21:605–631

DOI

114
Liang K, Liu F, Fan J(2017a) Nanoplasmonic quantification of tumour-derived extracellular vesicles in plasma microsamples for diagnosis and treatment monitoring. Nat Biomed Eng 1:0021

DOI

115
Liang L-G, Kong M-Q, Zhou S(2017b) An integrated doublefiltration microfluidic device for isolation, enrichment and quantification of urinary extracellular vesicles for detection of bladder cancer. Sci Rep 7:46224

DOI

116
Liégeois S, Benedetto A, Garnier J-M(2006) The V0-ATPase mediates apical secretion of exosomes containing Hedgehogrelated proteins in Caenorhabditis elegans. J Cell Biol 173:949–961

DOI

117
Liu C, Zhao J, Tian F(2019) Low-cost thermophoretic profiling of extracellular-vesicle surface proteins for the early detection and classification of cancers. Nat Biomed Eng 3:183–193

DOI

118
Liu F, Vermesh O, Mani V(2017a) The exosome total isolation chip. ACS Nano 11:10712–10723

DOI

119
Liu R, Wang X, Curtiss C(2018) Monoglyceride lipase gene knockout in mice leads to increased incidence of lung adenocarcinoma. Cell Death Dis 9:36

DOI

120
Liu X, Li Q, Niu X(2017b) Exosomes secreted from humaninduced pluripotent stem cell-derived mesenchymal stem cells prevent osteonecrosis of the femoral head by promoting angiogenesis. Int J Biol Sci 13:232–244

DOI

121
Logozzi M, Angelini DF, Iessi E(2017) Increased PSA expression on prostate cancer exosomes in in vitro condition and in cancer patients. Cancer Lett 403:318–329

DOI

122
Loh KM, van Amerongen R, Nusse R(2016) Generating cellular diversity and spatial form: Wnt signaling and the evolution of multicellular animals. Dev Cell 38:643–655

DOI

123
Lozano-Ramos I, Bancu I, Oliveira-Tercero A(2015) Sizeexclusion chromatography-based enrichment of extracellular vesicles from urine samples. J Extracell Vesicles 4:27369

DOI

124
Luan X, Sansanaphongpricha K, Myers I(2017) Engineering exosomes as refined biological nanoplatforms for drug delivery. Acta Pharmacol Sin 38:754–763

DOI

125
Ludwig N, Whiteside TL, Reichert TE(2019) Challenges in exosome isolation and analysis in health and disease. Int J Mol Sci 20:4684

DOI

126
Das S(2014) Extracellular vesicles in heart disease: excitement for the future? Exosomes Microvesicle. https://doi.org/10.5772/58390

DOI

127
Ma C, Jiang F, Ma Y(2019) Isolation and detection technologies of extracellular vesicles and application on cancer diagnostic. Dose-Response 17:155932581989100

DOI

128
Ma X, Yu H(2006) Global burden of cancer. Yale J Biol Med 79:85–94

129
Maas SLN, De Vrij J, Broekman MLD(2014) Quantification and sizeprofiling of extracellular vesicles using tunable resistive pulse sensing. J vis Exp. https://doi.org/10.3791/51623

DOI

130
Maguire JE, Silva M, Nguyen KCQ(2015) Myristoylated CIL-7 regulates ciliary extracellular vesicle biogenesis. Mol Biol Cell 26:2823–2832

DOI

131
Maia J, Caja S, Strano Moraes MC(2018) Exosome-based cellcell communication in the tumor microenvironment. Front Cell Dev Biol. https://doi.org/10.3389/fcell.2018.00018

DOI

132
Mao Y, Wang Y, Dong L(2019) Hypoxic exosomes facilitate angiogenesis and metastasis in esophageal squamous cell carcinoma through altering the phenotype and transcriptome of endothelial cells. J Exp Clin Cancer Res 38:389

DOI

133
Martin TA, Ye L, Sanders AJ(2013) Cancer invasion and metastasis: molecular and cellular perspective. In: Metastatic cancer: clinical and biological perspectives

134
Mašek J, Andersson ER(2017) The developmental biology of genetic Notch disorders. Development 144:1743–1763

DOI

135
Masyuk AI, Huang BQ, Ward CJ (2010) Biliary exosomes influence cholangiocyte regulatory mechanisms and proliferation through interaction with primary cilia. Am J Physiol Liver Physiol 299:G990–G999

DOI

136
Matusek T, Wendler F, Polès S(2014) The ESCRT machinery regulates the secretion and long-range activity of Hedgehog. Nature 516:99–103

DOI

137
McMahon AP, Hasso SM(2013) Filopodia: the cellular quills of Hedgehog signaling? Dev Cell 25:328–330

DOI

138
Melo SA, Luecke LB, Kahlert C(2015) Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature 523:177–182

DOI

139
Menck K, Scharf C, Bleckmann A (2015) Tumor-derived microvesicles mediate human breast cancer invasion through differentially glycosylated EMMPRIN. J Mol Cell Biol 7:143–153

DOI

140
Merchant ML, Rood IM, Deegens JKJ, Klein JB(2017) Isolation and characterization of urinary extracellular vesicles: implications for biomarker discovery. Nat Rev Nephrol 13:731–749

DOI

141
Minciacchi VR, Spinelli C, Reis-Sobreiro M (2017) MYC mediates large oncosome-induced fibroblast reprogramming in prostate cancer. Cancer Res 77:2306–2317

DOI

142
Momen-Heravi F(2017) Isolation of extracellular vesicles by ultracentrifugation. In: Methods in Molecular Biology. pp 25–32

DOI

143
Nakase I, Futaki S(2015) Combined treatment with a pH-sensitive fusogenic peptide and cationic lipids achieves enhanced cytosolic delivery of exosomes. Sci Rep 5:10112

DOI

144
Noble JM, Roberts LM, Vidavsky N (2020) Direct comparison of optical and electron microscopy methods for structural characterization of extracellular vesicles. J Struct Biol 210:107474

DOI

145
Ohlstein B, Kai T, Decotto E, Spradling A(2004) The stem cell niche: theme and variations. Curr Opin Cell Biol 16:693–699

DOI

146
Osteikoetxea X, Sódar B, Németh A (2015) Differential detergent sensitivity of extracellular vesicle subpopulations. Org Biomol Chem 13:9775–9782

DOI

147
Oszvald Á, Szvicsek Z, Sándor GO (2019) Extracellular vesicles transmit epithelial growth factor activity in the intestinal stem cell niche. Stem Cells. https://doi.org/10.1002/stem.3113

DOI

148
Othman N, Jamal R, Abu N(2019) Cancer-derived exosomes as effectors of key inflammation-related players. Front Immunol. https://doi.org/10.3389/fimmu.2019.02103

DOI

149
Palmieri V, Lucchetti D, Gatto I (2014) Dynamic light scattering for the characterization and counting of extracellular vesicles: a powerful noninvasive tool. J Nanoparticle Res 16:2583

DOI

150
Pan BT, Teng K, Wu C (1985) Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 101:942–948

DOI

151
Panáková D, Sprong H, Marois E(2005) Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435:58–65

DOI

152
Pang B, Zhu Y, Ni J (2020) Extracellular vesicles: the next generation of biomarkers for liquid biopsy-based prostate cancer diagnosis. Theranostics 10:2309–2326

DOI

153
Paolini L, Zendrini A, Radeghieri A(2018) Biophysical properties of extracellular vesicles in diagnostics. Biomark Med 12:383–391

DOI

154
Peinado H, Alečković M, Lavotshkin S (2012) Melanoma exosomes educate bone marrow progenitor cells toward a prometastatic phenotype through MET. Nat Med 18:883–891

DOI

155
Peinado H, Zhang H, Matei IR (2017) Pre-metastatic niches: organspecific homes for metastases. Nat Rev Cancer 17:302–317

DOI

156
Peng Y, Baulier E, Ke Y (2018) Human embryonic stem cells extracellular vesicles and their effects on immortalized human retinal Müller cells. PLoS ONE 13:e0194004

DOI

157
Pennings S, Liu KJ, Qian H(2018) The stem cell niche: interactions between stem cells and their environment. Stem Cells Int 2018:1–3

DOI

158
Plusa B, Hadjantonakis A-K(2014) Embryonic stem cell identity grounded in the embryo. Nat Cell Biol 16:502–504

DOI

159
Quesenberry PJ, Dooner MS, Aliotta JM(2010) Stem cell plasticity revisited: the continuum marrow model and phenotypic changes mediated by microvesicles. Exp Hematol 38:581–592

DOI

160
Raposo G, Nijman HW, Stoorvogel W (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183:1161–1172

DOI

161
Ratajczak J, Miekus K, Kucia M (2006) Embryonic stem cellderived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20:847–856

DOI

162
Ringborg U, Bergqvist D, Brorsson B(2003) The Swedish Council on Technology Assessment in Health Care (SBU) systematic overview of radiotherapy for cancer including a prospective survey of radiotherapy practice in Sweden 2001–summary and conclusions. Acta Oncol 42:357–365

DOI

163
Ronquist G, Brody I(1985) The prostasome: its secretion and function in man. Biochim Biophys Act 822:203–218

DOI

164
Rosa-Fernandes L, Rocha VB, Carregari VC(2017) A perspective on extracellular vesicles proteomics. Front Chem. https://doi.org/10.3389/fchem.2017.00102

DOI

165
Rozenblum P, Radrizzani (2019) Challenges in electrochemical aptasensors and current sensing architectures using flat gold surfaces. Chemosensors 7:57

DOI

166
Russell JC, Postupna N, Golubeva A(2020) Purification and analysis of Caenorhabditis elegans extracellular vesicles. J vis Exp. https://doi.org/10.3791/60596

DOI

167
Saenz-Antoñanzas A-I(2019) Liquid biopsy in glioblastoma: opportunities, applications and challenges. Cancers (basel) 11:950

DOI

168
Safdar A, Saleem A, Tarnopolsky MA(2016) The potential of endurance exercise-derived exosomes to treat metabolic diseases. Nat Rev Endocrinol 12:504–517

DOI

169
Sagar PF, Wiegreffe C, Scaal M(2015) Communication between distant epithelial cells by filopodia-like protrusions during embryonic development. Development 142:665–671

DOI

170
Salas-Vidal E, Lomeli H(2004) Imaging filopodia dynamics in the mouse blastocyst. Dev Biol 265:75–89

DOI

171
Salomon C, Kobayashi M, Tapia J(2015)Exosomes arefingerprints of originating cells: potential biomarkers for ovarian cancer. Res Reports Biochem. https://doi.org/10.2147/RRBC.S58281

DOI

172
Sandfeld-Paulsen B, Aggerholm-Pedersen N, Baek R(2016) Exosomal proteins as prognostic biomarkers in non-small cell lung cancer. Mol Oncol 10:1595–1602

DOI

173
Sato YT, Umezaki K, Sawada S(2016) Engineering hybrid exosomes by membrane fusion with liposomes. Sci Rep 6:21933

DOI

174
Savina A, Furlán M, Vidal M, Colombo MI(2003) Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem 278:20083–20090

DOI

175
Segura E, Nicco C, Lombard B(2005) ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 106:216–223

DOI

176
Sharma S, Das K, Woo J, Gimzewski JK(2014) Nanofilaments on glioblastoma exosomes revealed by peak force microscopy. J R Soc Interface 11:20131150

DOI

177
Sharma S, Gillespie BM, Palanisamy V, Gimzewski JK(2011) Quantitative nanostructural and single-molecule force spectroscopy biomolecular analysis of human-saliva-derived exosomes. Langmuir 27:14394–14400

DOI

178
Sharma S, LeClaire M, Gimzewski JK(2018) Ascent of atomic force microscopy as a nanoanalytical tool for exosomes and other extracellular vesicles. Nanotechnology 29:132001

DOI

179
Sharma S, Rasool HI, Palanisamy V(2010) Structuralmechanical characterization of nanoparticle exosomes in human saliva, using correlative AFM, FESEM, and force spectroscopy. ACS Nano 4:1921–1926

DOI

180
Sharma S, Zuñiga F, Rice GE (2017) Tumor-derived exosomes in ovarian cancer & liquid biopsies for early detection and realtime monitoring of cancer progression. Oncotarget. https://doi. org/10.18632/oncotarget.22191

DOI

181
Sheldon H, Heikamp E, Turley H (2010) New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood 116:2385–2394

DOI

182
Simons M, Raposo G(2009) Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol 21:575–581

DOI

183
Song M, Han L, Chen F(2018) Adipocyte-derived exosomes carrying Sonic Hedgehog mediate M1 macrophage polarizationinduced insulin resistance via Ptch and PI3K pathways. Cell Physiol Biochem 48:1416–1432

DOI

184
Soo CY, Song Y, Zheng Y (2012) Nanoparticle tracking analysis monitors microvesicle and exosome secretion from immune cells. Immunology 136:192–197

DOI

185
Soung Y, Ford S, Zhang V, Chung J(2017) Exosomes in cancer diagnostics. Cancers (basel) 9:8

DOI

186
Stahl PD, Raposo G (2018) Exosomes and extracellular vesicles: the path forward. Essays Biochem 62:119–124

DOI

187
Steeg PS(2016) Targeting metastasis. Nat Rev Cancer 16:201–218

DOI

188
Stronati E, Conti R, Cacci E(2019) Extracellular vesicleinduced differentiation of neural stem progenitor cells. Int J Mol Sci 20:3691

DOI

189
Subra C, Grand D, Laulagnier K(2010) Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J Lipid Res 51:2105–2120

DOI

190
Sun L, Xu R, Sun X(2016) Safety evaluation of exosomes derived from human umbilical cord mesenchymal stromal cell. Cytotherapy 18:413–422

DOI

191
Sun Z, Shi K, Yang S(2018) Effect of exosomal miRNA on cancer biology and clinical applications. Mol Cancer 17:147

DOI

192
Sverdlov ED(2012) Amedeo Avogadro’s cry: what is 1 μg of exosomes? BioEssays 34:873–875

DOI

193
Szatanek R, Baj-Krzyworzeka M, Zimoch J(2017) The methods of choice for extracellular vesicles (EVs) characterization. Int J Mol Sci 18:1153

DOI

194
Szatanek R, Baran J, Siedlar M, Baj-Krzyworzeka M(2015) Isolation of extracellular vesicles: determining the correct approach (Review). Int J Mol Med 36:11–17

DOI

195
Tai Y-L, Chu P-Y, Lee B-H(2019) Basics and applications of tumor-derived extracellular vesicles. J Biomed Sci 26:35

DOI

196
Takov K, Yellon DM, Davidson SM(2017) Confounding factors in vesicle uptake studies using fluorescent lipophilic membrane dyes. J Extracell Vesicles 6:1388731

DOI

197
Tanaka Y, Okada Y, Hirokawa N(2005) FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left–right determination. Nature 435:172–177

DOI

198
Teng X, Chen L, Chen W(2015) Mesenchymal stem cellderived exosomes improve the microenvironment of infracted myocardium contributing to angiogenesis and anti-inflammation. Cell Physiol Biochem 37:2415–2424

DOI

199
Thakur A(2019) The Study of Glioma-derived Exosomes as Biomarkers and Functional Mediators via MCT1, CD147, and CD44. City University of Hong Kong

200
Thakur A, Mishra AP, Panda B(2020a) Detection of disease specific parent cells via distinct population of nano-vesicles by machine learning. Curr Pharm Des. https://doi.org/10.2174/ 1381612826666200422091753

201
Thakur A, Mishra AP, Panda B, Majhi B(2020b) Application of artificial intelligence in pharmaceutical and biomedical studies. Curr Pharm Des. https://doi.org/10.2174/ 1381612826666200515131245

202
Thakur A, Qiu G(2017) Direct detection of two different tumorderived extracellular vesicles by SAM-AuNIs LSPR biosensor. Biosens Bioelectron 94:400–407

DOI

203
Thakur A, Qiu G, Xu C, (2020c) Label-free sensing of exosomal MCT1 and CD147 for tracking metabolic reprogramming and malignant progression in glioma. Sci Adv 6:eaaz6119

DOI

204
Thakur A, Sidu RK, Zou H(2020d) Inhibition of glioma cells’ proliferation by doxorubicin-loaded exosomes via microfluidics. Int J Nanomed 15:8331–8343

DOI

205
Thakur A, Zou H, Yang M, Lee Y(2018) Abstract 3720: Augmented loading efficiency of doxorubicin into glioma-derived exosomes by an integrated microfluidic device. In: Cancer Chemistry. American Association for Cancer Research, pp 3720–3720

DOI

206
Théry C, Amigorena S, Raposo G, Clayton A(2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 30:3.22.1–3.22.29

DOI

207
Théry C, Boussac M, Véron P(2001) Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 166:7309–7318

DOI

208
Théry C, Ostrowski M, Segura E(2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9:581–593

DOI

209
Théry C, Regnault A, Garin J(1999) Molecular characterization of dendritic cell-derived exosomes. J Cell Biol 147:599–610

DOI

210
Tian T, Zhang H-X, He C-P(2018) Surface functionalized exosomes as targeted drug delivery vehicles for cerebral ischemia therapy. Biomaterials 150:137–149

DOI

211
Tian W, Liu S, Li B(2019) Potential role of exosomes in cancer metastasis. Biomed Res Int 2019:1–12

DOI

212
Tonini T, Rossi F, Claudio PP(2003) Molecular basis of angiogenesis and cancer. Oncogene 22:6549–6556

DOI

213
Torregrosa Paredes P, Esser J, Admyre C(2012) Bronchoalveolar lavage fluid exosomes contribute to cytokine and leukotriene production in allergic asthma. Allergy 67:911–919

DOI

214
Tran C, Damaser MS(2015) Stem cells as drug delivery methods: application of stem cell secretome for regeneration. Adv Drug Deliv Rev 82–83:1–11

DOI

215
Vaidyanathan R, Naghibosadat M, Rauf S(2014) Detecting exosomes specifically: a multiplexed device based on alternating current electrohydrodynamic induced nanoshearing. Anal Chem 86:11125–11132

DOI

216
Vakhshiteh F, Atyabi F, Ostad SN(2019) Mesenchymal stem cell exosomes: a two-edged sword in cancer therapy. Int J Nanomedicine 14:2847–2859

DOI

217
Val S, Jeong S, Poley M(2017) Purification and characterization of microRNAs within middle ear fluid exosomes: implication in otitis media pathophysiology. Pediatr Res 81:911–918

DOI

218
van der Meel R, Fens MHAM, Vader P(2014) Extracellular vesicles as drug delivery systems: lessons from the liposome field. J Control Release 195:72–85

DOI

219
van der Pol E, Coumans FAW, Grootemaat AE(2014) Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost 12:1182–1192

DOI

220
Vasan N, Baselga J, Hyman DM(2019) A view on drug resistance in cancer. Nature 575:299–309

DOI

221
Viaud S, Terme M, Flament C(2009) Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: a role for NKG2D ligands and IL-15Rα. PLoS ONE 4:e4942

DOI

222
Waldenström A, Gennebäck N, Hellman U, Ronquist G(2012) Cardiomyocyte Microvesicles Contain DNA/RNA and Convey Biological Messages to Target Cells. PLoS ONE 7:e34653

DOI

223
Wang J, Silva M, Haas LA(2014a) C. elegans ciliated sensory neurons release extracellular vesicles that function in animal communication. Curr Biol 24:519–525

DOI

224
Wang L, Hu L, Zhou X(2017) Exosomes secreted by human adipose mesenchymal stem cells promote scarless cutaneous repair by regulating extracellular matrix remodelling. Sci Rep 7:13321

DOI

225
Wang RN, Green J, Wang Z(2014b) Bone Morphogenetic Protein (BMP) signaling in development and human diseases. Genes Dis 1:87–105

DOI

226
Wang Z, Wu H, Fine D(2013) Ciliated micropillars for the microfluidic-based isolation of nanoscale lipid vesicles. Lab Chip 13:2879

DOI

227
Wehman AM, Poggioli C, Schweinsberg P(2011) The P4-ATPase TAT-5 inhibits the budding of extracellular vesicles in C. elegans embryos. Curr Biol 21:1951–1959

DOI

228
Whitehead CA, Luwor RB, Morokoff AP(2017) Cancer exosomes in cerebrospinal fluid. Transl Cancer Res 6:S1352–S1370

DOI

229
Wiklander OPB, Brennan MÁ, Lötvall J(2019) Advances in therapeutic applications of extracellular vesicles. Sci Transl Med 11:eaav8521

DOI

230
Witwer KW, Buzás EI, Bemis LT(2013) Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2:20360

DOI

231
Woo H-K, Sunkara V, Park J(2017) Exodisc for rapid, sizeselective, and efficient isolation and analysis of nanoscale extracellular vesicles from biological samples. ACS Nano 11:1360–1370

DOI

232
Wood CR, Rosenbaum JL(2015) Ciliary ectosomes: transmissions from the cell’s antenna. Trends Cell Biol 25:276–285

DOI

233
Wu J, Qu Z, Fei Z-W(2017) Role of stem cell-derived exosomes in cancer. Oncol Lett 13:2855–2866

DOI

234
Wu Y, Deng W, Klinke DJII (2015) Exosomes: improved methods to characterize their morphology, RNA content, and surface protein biomarkers. Analyst 140:6631–6642

DOI

235
Wunsch BH, Smith JT, Gifford SM(2016) Nanoscale lateral displacement arrays for the separation of exosomes and colloids down to 20 nm. Nat Nanotechnol 11:936–940

DOI

236
Xia Y, Liu M, Wang L(2017) A visible and colorimetric aptasensor based on DNA-capped single-walled carbon nanotubes for detection of exosomes. Biosens Bioelectron 92:8–15

DOI

237
Xu R, Greening DW, Zhu H-J(2016) Extracellular vesicle isolation and characterization: toward clinical application. J Clin Invest 126:1152–1162

DOI

238
Yamashita T, Takahashi Y, Takakura Y(2018) Possibility of exosome-based therapeutics and challenges in production of exosomes eligible for therapeutic application. Biol Pharm Bull 41:835–842

DOI

239
Yao X, Wei W, Wang X(2019) Stem cell derived exosomes: microRNA therapy for age-related musculoskeletal disorders. Biomaterials 224:119492

DOI

240
Yokoyama S, Takeuchi A, Yamaguchi S(2017) Clinical implications of carcinoembryonic antigen distribution in serum exosomal fraction—measurement by ELISA. PLoS ONE 12: e0183337

DOI

241
Yu L-L, Zhu J, Liu J-X(2018) A comparison of traditional and novel methods for the separation of exosomes from human samples. Biomed Res Int 2018:1–9

DOI

242
Yu X, Deng L, Wang D(2012) Mechanism of TNF-α autocrine effects in hypoxic cardiomyocytes: initiated by hypoxia inducible factor 1α, presented by exosomes. J Mol Cell Cardiol 53:848–857

DOI

243
Yuana Y, Oosterkamp TH, Bahatyrova S(2010) Atomic force microscopy: a novel approach to the detection of nanosized blood microparticles. J Thromb Haemost 8:315–323

DOI

244
Zhang H, Jiang L-H, Hou J-C(2018) Exosome: a novel mediator in drug resistance of cancer cells. Epigenomics 10:1499–1509

DOI

245
Zhang M, Vojtech L, Ye Z(2020) Quantum dot labeling and visualization of extracellular vesicles. ACS Appl Nano Mater 3:7211–7222

DOI

246
Zhang P, He M, Zeng Y(2016a) Ultrasensitive microfluidic analysis of circulating exosomes using a nanostructured graphene oxide/ polydopamine coating. Lab Chip 16:3033–3042

DOI

247
Zhang W, Yu Z-L, Wu M(2017) Magnetic and folate functionalization enables rapid isolation and enhanced tumortargeting of cell-derived microvesicles. ACS Nano 11:277–290

DOI

248
Zhang Y, Liu Y, Liu H, Tang WH(2019) Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci 9:19

DOI

249
Zhang Y, Yu Z, Jiang D(2016b) iPSC-MSCs with high intrinsic MIRO1 and sensitivity to TNF-α yield efficacious mitochondrial transfer to rescue anthracycline-induced cardiomyopathy. Stem Cell Rep 7:749–763

DOI

250
Zhao Z, Yang Y, Zeng Y, He M(2016) A microfluidic ExoSearch chip for multiplexed exosome detection towards blood-based ovarian cancer diagnosis. Lab Chip 16:489–496

DOI

251
Zhou Q, Rahimian A, Son K(2016) Development of an aptasensor for electrochemical detection of exosomes. Methods 97:88–93

DOI

252
Zhu Q, Heon M, Zhao Z, He M(2018) Microfluidic engineering of exosomes: editing cellular messages for precision therapeutics. Lab Chip 18:1690–1703

DOI

253
Zhu Q, Ling X, Yang Y(2019) Embryonic stem cells-derived exosomes endowed with targeting properties as chemotherapeutics delivery vehicles for glioblastoma therapy. Adv Sci 6:1801899

DOI

254
Zitvogel L, Regnault A, Lozier A(1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell derived exosomes. Nat Med 4:594–600

DOI

255
(2018) P30: Uptake of trophoblast extracellular vesicles by neighboring cells. Am J Reprod Immunol 80:71–71

DOI

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