Skip to main content

Advertisement

Log in

An update in the applications of exosomes in cancer theranostics: from research to clinical trials

  • Review
  • Published:
Journal of Cancer Research and Clinical Oncology Aims and scope Submit manuscript

Abstract

Exosomes are nanosized extracellular vesicles secreted by nearly all viable cells following the fusing of multivesicular bodies and the plasma membrane and discharged into the encircling bodily fluids. Exosomes can transport cell-specific components from the source cell to the target cell. Given the enormous potential of exosomes as non-invasive diagnostic biomarkers and therapeutic nanovehicles. Lately, accumulated evidence has demonstrated that exosomes serve an important role in prognosis, diagnosis, and even treatment strategies. While several reviews have collective information on the biomedical application of exosomes, a comprehensive review incorporating updated and improved methodologies for beneficial applications of such vesicles in cancer theranostics is indispensable. In the current review, we first provided a comprehensive review of the introduction of exosomes, featuring their discovery, separation, characterization, function, biogenesis, secretion. The implications of exosomes as promising nanovehicles for drug and gene delivery, application of exosome inhibitors in the management of cancers, completed and ongoing clinical trials on the biological relevance of exosomes are then discussed in detail. As the field of exosome research grows, a better understanding of the subcellular parts and mechanisms involved in exosome secretion and targeting of specific cells will help figure out what their exact physiological functions are in the body.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of data and materials

Not applicable.

References

  • Adams LS, Phung S, Chen S (2011) Blueberry phytochemicals inhibit growth and metastatic potential of MDA-MB-231 breast cancer cells through modulation of the phosphatidylinositol 3-kinase pathway. Wiley Online Library

    Google Scholar 

  • Agrawal AK, Aqil F, Jeyabalan J, Spencer WA, Beck J, Gachuki BW, Alhakeem SS, Oben K, Munagala R, Bondada S (2017) Milk-derived exosomes for oral delivery of paclitaxel. Nanomed: Nanotechnol Biol Med 13(5):1627–1636

    CAS  Google Scholar 

  • Airola MV, Shanbhogue P, Shamseddine AA, Guja KE, Senkal CE, Maini R, Bartke N, Wu BX, Obeid LM, Garcia-Diaz M (2017) Structure of human nSMase2 reveals an interdomain allosteric activation mechanism for ceramide generation. Proc Natl Acad Sci 114(28):E5549–E5558

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aqil F, Kausar H, Agrawal AK, Jeyabalan J, Kyakulaga A-H, Munagala R, Gupta R (2016) Exosomal formulation enhances therapeutic response of celastrol against lung cancer. Exp Mol Pathol 101(1):12–21

    CAS  PubMed  Google Scholar 

  • Aqil F, Jeyabalan J, Agrawal AK, Kyakulaga A-H, Munagala R, Parker L, Gupta RC (2017) Exosomal delivery of berry anthocyanidins for the management of ovarian cancer. Food Funct 8(11):4100–4107

    CAS  PubMed  Google Scholar 

  • Aqil F, Munagala R, Jeyabalan J, Agrawal AK, Kyakulaga A-H, Wilcher SA, Gupta RC (2019) Milk exosomes-natural nanoparticles for siRNA delivery. Cancer Lett 449:186–195

    CAS  PubMed  Google Scholar 

  • Arenz C, Gartner M, Wascholowski V, Giannis A (2001) Synthesis and biochemical investigation of scyphostatin analogues as inhibitors of neutral sphingomyelinase. Bioorg Med Chem 9(11):2901–2904

    CAS  PubMed  Google Scholar 

  • Arshad R, Fatima I, Sargazi S, Rahdar A, Karamzadeh-Jahromi M, Pandey S, Díez-Pascual AM, Bilal M (2021) Novel perspectives towards RNA-based nano-theranostic approaches for cancer management. Nanomaterials 11(12):3330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bai J, Duan J, Liu R, Du Y, Luo Q, Cui Y, Su Z, Xu J, Xie Y, Lu W (2020) Engineered targeting tLyp-1 exosomes as gene therapy vectors for efficient delivery of siRNA into lung cancer cells. Asian J Pharm Sci 15(4):461–471

    PubMed  Google Scholar 

  • Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E (2012) Syndecan–syntenin–ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14(7):677–685

    CAS  PubMed  Google Scholar 

  • Barceló M, Castells M, Bassas L, Vigués F, Larriba S (2019) Semen miRNAs contained in exosomes as non-invasive biomarkers for prostate cancer diagnosis. Sci Rep 9(1):1–16

    Google Scholar 

  • Bebelman MP, Smit MJ, Pegtel DM, Baglio SR (2018) Biogenesis and function of extracellular vesicles in cancer. Pharmacol Ther 188:1–11

    CAS  PubMed  Google Scholar 

  • Bobrie A, Colombo M, Raposo G, Théry C (2011) Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 12(12):1659–1668

    CAS  PubMed  Google Scholar 

  • Byrne M, Tzekov R, Wang Y, Rodgers A, Cardia J, Ford G, Holton K, Pandarinathan L, Lapierre J, Stanney W (2013) Novel hydrophobically modified asymmetric RNAi compounds (sd-rxRNA) demonstrate robust efficacy in the eye. J Ocul Pharmacol Ther 29(10):855–864

    CAS  PubMed  Google Scholar 

  • Campanella C, Rappa F, Sciumè C, Marino Gammazza A, Barone R, Bucchieri F, David S, Curcurù G, Caruso Bavisotto C, Pitruzzella A (2015) Heat shock protein 60 levels in tissue and circulating exosomes in human large bowel cancer before and after ablative surgery. Cancer 121(18):3230–3239

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Canitano A, Iessi E, Spugnini EP, Federici C, Fais S (2016) Proton pump inhibitors induce a caspase-independent antitumor effect against human multiple myeloma. Cancer Lett 376(2):278–283

    CAS  PubMed  Google Scholar 

  • Chen Y, Gao D-Y, Huang L (2015) In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv Drug Deliv Rev 81:128–141

    CAS  PubMed  Google Scholar 

  • Chen J, Li P, Zhang T, Xu Z, Huang X, Wang R, Du L (2022) Review on strategies and technologies for exosome isolation and purification. Front Bioeng Biotechnol 9:811971

    PubMed  PubMed Central  Google Scholar 

  • Chitra R, Harikumar KB (2018) The origin and functions of exosomes in cancer. Front Oncol. https://doi.org/10.3389/fonc.2018.00066

    Article  Google Scholar 

  • Cho S, Yang HC, Rhee WJ (2019) Simultaneous multiplexed detection of exosomal microRNAs and surface proteins for prostate cancer diagnosis. Biosens Bioelectron 146:111749

    CAS  PubMed  Google Scholar 

  • Clark DJ, Fondrie WE, Liao Z, Hanson PI, Fulton A, Mao L, Yang AJ (2015) Redefining the breast cancer exosome proteome by tandem mass tag quantitative proteomics and multivariate cluster analysis. Anal Chem 87(20):10462–10469

    CAS  PubMed  PubMed Central  Google Scholar 

  • Colao IL, Corteling R, Bracewell D, Wall I (2018) Manufacturing exosomes: a promising therapeutic platform. Trends Mol Med 24(3):242–256

    CAS  PubMed  Google Scholar 

  • Colombo M, Moita C, Van Niel G, Kowal J, Vigneron J, Benaroch P, Manel N, Moita LF, 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(24):5553–5565

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Console L, Scalise M, Indiveri C (2019) Exosomes in inflammation and role as biomarkers. Clin Chim Acta 488:165–171

    CAS  PubMed  Google Scholar 

  • Dash M, Palaniyandi K, Ramalingam S, Sahabudeen S, Raja N (2021) Exosomes isolated from two different cell lines using three different isolation techniques show variation in physical and molecular characteristics. Biochim Biophys Acta (BBA)-Biomembr 1863(2):183490

    CAS  Google Scholar 

  • Datta A, Kim H, Lal M, McGee L, Johnson A, Moustafa AA, Jones JC, Mondal D, Ferrer M, Abdel-Mageed AB (2017) Manumycin A suppresses exosome biogenesis and secretion via targeted inhibition of Ras/Raf/ERK1/2 signaling and hnRNP H1 in castration-resistant prostate cancer cells. Cancer Lett 408:73–81

    CAS  PubMed  PubMed Central  Google Scholar 

  • Datta A, Kim H, McGee L, Johnson AE, Talwar S, Marugan J, Southall N, Hu X, Lal M, Mondal D (2018) High-throughput screening identified selective inhibitors of exosome biogenesis and secretion: a drug repurposing strategy for advanced cancer. Sci Rep 8(1):1–13

    CAS  Google Scholar 

  • De Rosa G, Salzano G, Caraglia M, Abbruzzese A (2012) Nanotechnologies: a strategy to overcome blood-brain barrier. Curr Drug Metab 13(1):61–69

    PubMed  Google Scholar 

  • 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 6:203

    PubMed  PubMed Central  Google Scholar 

  • Denny WA, Wilson WR (2000) Tirapazamine: a bioreductive anticancer drug that exploits tumour hypoxia. Expert Opin Investig Drugs 9(12):2889–2901

    CAS  PubMed  Google Scholar 

  • Didiot M-C, Hall LM, Coles AH, Haraszti RA, Godinho BM, Chase K, Sapp E, Ly S, Alterman JF, Hassler MR (2016) Exosome-mediated delivery of hydrophobically modified siRNA for huntingtin mRNA silencing. Mol Ther 24(10):1836–1847

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dijkstra S, Birker IL, Smit FP, Leyten GH, de Reijke TM, van Oort IM, Mulders PF, Jannink SA, Schalken JA (2014) Prostate cancer biomarker profiles in urinary sediments and exosomes. J Urol 191(4):1132–1138

    CAS  PubMed  Google Scholar 

  • Essandoh K, Yang L, Wang X, Huang W, Qin D, Hao J, Wang Y, Zingarelli B, Peng T, Fan G-C (2015) Blockade of exosome generation with GW4869 dampens the sepsis-induced inflammation and cardiac dysfunction. Biochim Biophys Acta (BBA)-Mol Basis Dis 1852(11):2362–2371

    CAS  Google Scholar 

  • Fais S (2015) Evidence-based support for the use of proton pump inhibitors in cancer therapy. J Transl Med 13(1):1–5

    Google Scholar 

  • Federici C, Petrucci F, Caimi S, Cesolini A, Logozzi M, Borghi M, D’Ilio S, Lugini L, Violante N, Azzarito T (2014) Exosome release and low pH belong to a framework of resistance of human melanoma cells to cisplatin. PLoS ONE 9(2):e88193

    PubMed  PubMed Central  Google Scholar 

  • Février B, Raposo G (2004) Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 16(4):415–421

    PubMed  Google Scholar 

  • Figuera-Losada M, Stathis M, Dorskind JM, Thomas AG, Bandaru VVR, Yoo S-W, Westwood NJ, Rogers GW, McArthur JC, Haughey NJ (2015) Cambinol, a novel inhibitor of neutral sphingomyelinase 2 shows neuroprotective properties. PLoS ONE 10(5):e0124481

    PubMed  PubMed Central  Google Scholar 

  • Fuhrmann G, Serio A, Mazo M, Nair R, Stevens MM (2015) Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins. J Control Release 205:35–44

    CAS  PubMed  Google Scholar 

  • Gangoda L, Boukouris S, Liem M, Kalra H, Mathivanan S (2015) Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics 15(2–3):260–271

    CAS  PubMed  Google Scholar 

  • Gao Z, Yuan H, Mao Y, Ding L, Effah CY, He S, He L, Liu L-E, Yu S, Wang Y (2021) In situ detection of plasma exosomal microRNA for lung cancer diagnosis using duplex-specific nuclease and MoS 2 nanosheets. Analyst 146(6):1924–1931

    CAS  PubMed  Google Scholar 

  • Gong C, Tian J, Wang Z, Gao Y, Wu X, Ding X, Qiang L, Li G, Han Z, Yuan Y (2019) Functional exosome-mediated co-delivery of doxorubicin and hydrophobically modified microRNA 159 for triple-negative breast cancer therapy. J Nanobiotechnol 17(1):1–18

    CAS  Google Scholar 

  • Groot M, Lee H (2020) Sorting mechanisms for MicroRNAs into extracellular vesicles and their associated diseases. Cells 9(4):1044

    CAS  PubMed  PubMed Central  Google Scholar 

  • György B, Szabó TG, Pásztói M, Pál Z, Misják P, Aradi B, László V, Pállinger E, Pap E, Kittel A (2011) Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 68(16):2667–2688

    PubMed  PubMed Central  Google Scholar 

  • Haney MJ, Suresh P, Zhao Y, Kanmogne GD, Kadiu I, Sokolsky-Papkov M, Klyachko NL, Mosley RL, Kabanov AV, Gendelman HE (2012) Blood-borne macrophage–neural cell interactions hitchhike on endosome networks for cell-based nanozyme brain delivery. Nanomedicine 7(6):815–833

    CAS  PubMed  Google Scholar 

  • Haney MJ, Zhao Y, Harrison EB, Mahajan V, Ahmed S, He Z, Suresh P, Hingtgen SD, Klyachko NL, Mosley RL (2013) Specific transfection of inflamed brain by macrophages: a new therapeutic strategy for neurodegenerative diseases. PLoS ONE 8(4):e61852

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, Patel T, Piroyan A, Sokolsky M, Kabanov AV (2015) Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release 207:18–30

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hannafon BN, Trigoso YD, Calloway CL, Zhao YD, Lum DH, Welm AL, Zhao ZJ, Blick KE, Dooley WC, Ding W (2016) Plasma exosome microRNAs are indicative of breast cancer. Breast Cancer Res 18(1):1–14

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hessvik NP, Llorente A (2018) Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 75(2):193–208

    CAS  PubMed  Google Scholar 

  • Hong W, Chen Y, You K, Tan S, Wu F, Tao J, Chen X, Zhang J, Xiong Y, Yuan F (2020) Celebrex adjuvant therapy on coronavirus disease 2019: an experimental study. Front Pharmacol. https://doi.org/10.3389/fphar.2020.561674

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoshino A, Costa-Silva B, Shen T-L, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S (2015) Tumour exosome integrins determine organotropic metastasis. Nature 527(7578):329–335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang L, Rong Y, Tang X, Yi K, Wu J, Wang F (2021) Circular RNAs are promising biomarkers in liquid biopsy for the diagnosis of non-small cell lung cancer. Front Mol Biosci 8:625722

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hulsmans M, Holvoet P (2013) MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease. Cardiovasc Res 100(1):7–18

    CAS  PubMed  Google Scholar 

  • Im E-J, Lee C-H, Moon P-G, Rangaswamy GG, Lee B, Lee JM, Lee J-C, Jee J-G, Bae J-S, Kwon T-K (2019) Sulfisoxazole inhibits the secretion of small extracellular vesicles by targeting the endothelin receptor A. Nat Commun 10(1):1–17

    CAS  Google Scholar 

  • Jeong K, Yu YJ, You JY, Rhee WJ, Kim JA (2020) Exosome-mediated microRNA-497 delivery for anti-cancer therapy in a microfluidic 3D lung cancer model. Lab Chip 20(3):548–557

    CAS  PubMed  Google Scholar 

  • Jiang L, Vader P, Schiffelers R (2017) Extracellular vesicles for nucleic acid delivery: progress and prospects for safe RNA-based gene therapy. Gene Ther 24(3):157–166

    CAS  PubMed  Google Scholar 

  • Jin HZ, Hwang BY, Kim HS, Lee JH, Kim YH, Lee JJ (2002) Antiinflammatory constituents of celastrus o rbiculatus inhibit the NF-κB activation and NO production. J Nat Prod 65(1):89–91

    CAS  PubMed  Google Scholar 

  • Johnson JL, Ramadass M, He J, Brown SJ, Zhang J, Abgaryan L, Biris N, Gavathiotis E, Rosen H, Catz SD (2016) Identification of neutrophil exocytosis inhibitors (Nexinhibs), small molecule inhibitors of neutrophil exocytosis and inflammation: druggability of the small GTPase Rab27a. J Biol Chem 291(50):25965–25982

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kalluri R (2016) The biology and function of exosomes in cancer. J Clin Investig 126(4):1208–1215

    PubMed  PubMed Central  Google Scholar 

  • Kalluri R, LeBleu VS (2020) The biology, function, and biomedical applications of exosomes. Science 367(6478):eaau6977

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kausar H, Jeyabalan J, Aqil F, Chabba D, Sidana J, Singh IP, Gupta RC (2012) Berry anthocyanidins synergistically suppress growth and invasive potential of human non-small-cell lung cancer cells. Cancer Lett 325(1):54–62

    CAS  PubMed  Google Scholar 

  • Keller S, Sanderson MP, Stoeck A, Altevogt P (2006) Exosomes: from biogenesis and secretion to biological function. Immunol Lett 107(2):102–108

    CAS  PubMed  Google Scholar 

  • Khan FM, Saleh E, Alawadhi H, Harati R, Zimmermann W-H, El-Awady R (2018) Inhibition of exosome release by ketotifen enhances sensitivity of cancer cells to doxorubicin. Cancer Biol Ther 19(1):25–33

    CAS  PubMed  Google Scholar 

  • Kim H, Rhee WJ (2020) Exosome-mediated let7c-5p delivery for breast cancer therapeutic development. Biotechnol Bioprocess Eng 25(4):513–520

    CAS  Google Scholar 

  • Kim D-K, Kang B, Kim OY, Choi D-S, Lee J, Kim SR, Go G, Yoon YJ, Kim JH, Jang SC (2013) EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles. J Extracell Vesicles 2(1):20384

    Google Scholar 

  • Kim R, Lee S, Lee J, Kim M, Kim WJ, Lee HW, Lee MY, Kim J, Chang W (2018) Exosomes derived from microRNA-584 transfected mesenchymal stem cells: novel alternative therapeutic vehicles for cancer therapy. BMB Rep 51(8):406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kirave P, Gondaliya P, Kulkarni B, Rawal R, Garg R, Jain A, Kalia K (2020) Exosome mediated miR-155 delivery confers cisplatin chemoresistance in oral cancer cells via epithelial-mesenchymal transition. Oncotarget 11(13):1157

    PubMed  PubMed Central  Google Scholar 

  • Kobayashi M, Sawada K, Miyamoto M, Shimizu A, Yamamoto M, Kinose Y, Nakamura K, Kawano M, Kodama M, Hashimoto K (2020) Exploring the potential of engineered exosomes as delivery systems for tumor-suppressor microRNA replacement therapy in ovarian cancer. Biochem Biophys Res Commun 527(1):153–161

    CAS  PubMed  Google Scholar 

  • Kosgodage US, Mould R, Henley AB, Nunn AV, Guy GW, Thomas EL, Inal JM, Bell JD, Lange S (2018) Cannabidiol (CBD) is a novel inhibitor for exosome and microvesicle (EMV) release in cancer. Front Pharmacol 9:889

    PubMed  PubMed Central  Google Scholar 

  • Kouzegaran S, Shahraki K, Makateb A, Shahri F, Hatami N, Behnod V, Tanha AS (2017) Prognostic investigations of expression level of two genes FasL and Ki-67 as independent prognostic markers of human retinoblastoma. Oncol Res 25(4):471

    PubMed  PubMed Central  Google Scholar 

  • Kowalczuk L, Matet A, Dor M, Bararpour N, Daruich A, Dirani A, Behar-Cohen F, Thomas A, Turck N (2018) Proteome and metabolome of subretinal fluid in central serous chorioretinopathy and rhegmatogenous retinal detachment: a pilot case study. Transl vis Sci Technol 7(1):3–3

    PubMed  PubMed Central  Google Scholar 

  • Kulshreshtha A, Singh S, Ahmad M, Khanna K, Ahmad T, Agrawal A, Ghosh B (2019) Simvastatin mediates inhibition of exosome synthesis, localization and secretion via multicomponent interventions. Sci Rep 9(1):1–10

    CAS  Google Scholar 

  • Lallemand T, Rouahi M, Swiader A, Grazide M-H, Geoffre N, Alayrac P, Recazens E, Coste A, Salvayre R, Nègre-Salvayre A (2018) nSMase2 (type 2-neutral sphingomyelinase) deficiency or inhibition by GW4869 reduces inflammation and atherosclerosis in Apoe−/− mice. Arterioscler Thromb Vasc Biol 38(7):1479–1492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laraib U, Sargazi S, Rahdar A, Khatami M, Pandey S (2021) Nanotechnology-based approaches for effective detection of tumor markers: a comprehensive state-of-the-art review. Int J Biol Macromol. https://doi.org/10.1016/j.ijbiomac.2021.12.052

    Article  PubMed  Google Scholar 

  • Lee J, Lee H, Goh U, Kim J, Jeong M, Lee J, Park J-H (2016) Cellular engineering with membrane fusogenic liposomes to produce functionalized extracellular vesicles. ACS Appl Mater Interfaces 8(11):6790–6795

    CAS  PubMed  Google Scholar 

  • Leidal AM, Debnath J (2020) Unraveling the mechanisms that specify molecules for secretion in extracellular vesicles. Methods 177:15–26

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Zheng Q, Bao C, Li S, Guo W, Zhao J, Chen D, Gu J, He X, Huang S (2015) Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res 25(8):981–984

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Wang H, Yin H, Bennett C, Zhang H-G, Guo P (2018) Arrowtail RNA for ligand display on ginger exosome-like nanovesicles to systemic deliver siRNA for cancer suppression. Sci Rep 8(1):1–11

    Google Scholar 

  • Lin S, Yu Z, Chen D, Wang Z, Miao J, Li Q, Zhang D, Song J, Cui D (2020) Progress in microfluidics-based exosome separation and detection technologies for diagnostic applications. Small 16(9):1903916

    CAS  Google Scholar 

  • Lin D, Zhang H, Liu R, Deng T, Ning T, Bai M, Yang Y, Zhu K, Wang J, Duan J (2021) iRGD-modified exosomes effectively deliver CPT1A siRNA to colon cancer cells, reversing oxaliplatin resistance by regulating fatty acid oxidation. Mol Oncol 15(12):3430–3446

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lobb RJ, Lima LG, Möller A (2017) Exosomes: key mediators of metastasis and pre-metastatic niche formation. Semin Cell Dev Biol 67:3–10

    CAS  PubMed  Google Scholar 

  • Logozzi M, Mizzoni D, Angelini DF, Di Raimo R, Falchi M, Battistini L, Fais S (2018) Microenvironmental pH and exosome levels interplay in human cancer cell lines of different histotypes. Cancers 10(10):370

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lott K, Li J, Fisk JC, Wang H, Aletta JM, Qu J, Read LK (2013) Global proteomic analysis in trypanosomes reveals unique proteins and conserved cellular processes impacted by arginine methylation. J Proteomics 91:210–225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lou W, Liu J, Gao Y, Zhong G, Chen D, Shen J, Bao C, Xu L, Pan J, Cheng J (2017) MicroRNAs in cancer metastasis and angiogenesis. Oncotarget 8:115787–115802

    PubMed  PubMed Central  Google Scholar 

  • Lovell JF, Jin CS, Huynh E, Jin H, Kim C, Rubinstein JL, Chan WC, Cao W, Wang LV, Zheng G (2011) Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nat Mater 10(4):324–332

    CAS  PubMed  Google Scholar 

  • Luberto C, Hassler DF, Signorelli P, Okamoto Y, Sawai H, Boros E, Hazen-Martin DJ, Obeid LM, Hannun YA, Smith GK (2002) Inhibition of tumor necrosis factor-induced cell death in MCF7 by a novel inhibitor of neutral sphingomyelinase. J Biol Chem 277(43):41128–41139

    CAS  PubMed  Google Scholar 

  • Luciani F, Spada M, De Milito A, Molinari A, Rivoltini L, Montinaro A, Marra M, Lugini L, Logozzi M, Lozupone F (2004) Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J Natl Cancer Inst 96(22):1702–1713

    CAS  PubMed  Google Scholar 

  • Machida T, Tomofuji T, Maruyama T, Yoneda T, Ekuni D, Azuma T, Miyai H, Mizuno H, Kato H, Tsutsumi K (2016) miR-1246 and miR-4644 in salivary exosome as potential biomarkers for pancreatobiliary tract cancer. Oncol Rep 36(4):2375–2381

    CAS  PubMed  Google Scholar 

  • Madhavan B, Yue S, Galli U, Rana S, Gross W, Müller M, Giese NA, Kalthoff H, Becker T, Büchler MW (2015) Combined evaluation of a panel of protein and miRNA serum-exosome biomarkers for pancreatic cancer diagnosis increases sensitivity and specificity. Int J Cancer 136(11):2616–2627

    CAS  PubMed  Google Scholar 

  • Manicum A-LE, Sargazi S, Razzaq S, Kumar GV, Rahdar A, Er S, Ain QU, Bilal M, Aboudzadeh MA (2022) Nano-immunotherapeutic strategies for targeted RNA delivery: Emphasizing the role of monocyte/macrophages as nanovehicles to treat glioblastoma multiforme. J Drug Deliv Sci Technol 71:103288

    Google Scholar 

  • Martin L-A, Head JE, Pancholi S, Salter J, Quinn E, Detre S, Kaye S, Howes A, Dowsett M, Johnston SR (2007) The farnesyltransferase inhibitor R115777 (tipifarnib) in combination with tamoxifen acts synergistically to inhibit MCF-7 breast cancer cell proliferation and cell cycle progression in vitro and in vivo. Mol Cancer Ther 6(9):2458–2467

    CAS  PubMed  Google Scholar 

  • Mateescu B, Kowal EJ, van Balkom BW, Bartel S, Bhattacharyya SN, Buzás EI, Buck AH, de Candia P, Chow FW, Das S (2017) Obstacles and opportunities in the functional analysis of extracellular vesicle RNA–an ISEV position paper. Journal of Extracellular Vesicles 6(1):1286095

    PubMed  PubMed Central  Google Scholar 

  • Mathivanan S, Fahner CJ, Reid GE, Simpson RJ (2012) ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res 40(D1):D1241–D1244

    CAS  PubMed  Google Scholar 

  • Möbius W, Ohno-Iwashita Y, Donselaar EGV, 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

    PubMed  Google Scholar 

  • Muralidharan-Chari V, Clancy JW, Sedgwick A, D’Souza-Schorey C (2010) Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123(10):1603–1611

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nara F, Tanaka M, Masuda-Inoue S, Yamasato Y, Doi-Yoshioka H, Suzuki-Konagai K, Kumakura S, Ogita T (1999) Biological activities of scyphostatin, a neutral sphingomyelinase inhibitor from a discomycete, Trichopeziza mollissima. J Antibiot 52(6):531–535

    CAS  Google Scholar 

  • Nazarenko I, Rupp A-K, Altevogt P (2013) Exosomes as a potential tool for a specific delivery of functional molecules. Springer, Ovarian Cancer, pp 495–511

    Google Scholar 

  • Nuzhat Z, Kinhal V, Sharma S, Rice GE, Joshi V, Salomon C (2017) Tumour-derived exosomes as a signature of pancreatic cancer-liquid biopsies as indicators of tumour progression. Oncotarget 8(10):17279

    PubMed  Google Scholar 

  • Ogorevc E, Kralj-Iglic V, Veranic P (2013) The role of extracellular vesicles in phenotypic cancer transformation. Radiol Oncol 47(3):197–205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohno S-I, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, Fujita K, Mizutani T, Ohgi T, Ochiya T (2013) Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 21(1):185–191

    CAS  PubMed  Google Scholar 

  • Ohno S-I, Drummen GP, Kuroda M (2016) Focus on extracellular vesicles: development of extracellular vesicle-based therapeutic systems. Int J Mol Sci 17(2):172

    PubMed  PubMed Central  Google Scholar 

  • Oosthuyzen W, Sime NE, Ivy JR, Turtle EJ, Street JM, Pound J, Bath LE, Webb DJ, Gregory CD, Bailey MA (2013) Quantification of human urinary exosomes by nanoparticle tracking analysis. J Physiol 591(23):5833–5842

    CAS  PubMed  PubMed Central  Google Scholar 

  • Papa A, Wan L, Bonora M, Salmena L, Song MS, Hobbs RM, Lunardi A, Webster K, Ng C, Newton RH (2014) Cancer-associated PTEN mutants act in a dominant-negative manner to suppress PTEN protein function. Cell 157(3):595–610

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, Coscia C, Iessi E, Logozzi M, Molinari A (2009) Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 284(49):34211–34222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Patil AA, Rhee WJ (2019) Exosomes: biogenesis, composition, functions, and their role in pre-metastatic niche formation. Biotechnol Bioprocess Eng 24(5):689–701

    CAS  Google Scholar 

  • Phinney D, Pittenger M (2017) MSC-derived exosomes for cell-free therapy. Stem Cells 35:851–858

    CAS  PubMed  Google Scholar 

  • Pocsfalvi G, Stanly C, Vilasi A, Fiume I, Capasso G, Turiák L, Buzas EI, Vékey K (2016) Mass spectrometry of extracellular vesicles. Mass Spectrom Rev 35(1):3–21

    CAS  PubMed  Google Scholar 

  • Qindeel M, Sabir F, Sargazi S, Mohammadzadeh V, Mulla SI (2021) New insights into the application of nanoghosts as theranostic tools with an emphasis on cardiovascular diseases. J Nanopart Res 23(11):1–27

    Google Scholar 

  • Raimondo F, Morosi L, Chinello C, Magni F, Pitto M (2011) Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery. Proteomics 11(4):709–720

    CAS  PubMed  Google Scholar 

  • Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200(4):373–383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Record M, Carayon K, Poirot M, Silvente-Poirot S (2014) Exosomes as new vesicular lipid transporters involved in cell–cell communication and various pathophysiologies. Biochim Biophys Acta (BBA)-Mol Cell Biol Lipids 1841(1):108–120

    CAS  Google Scholar 

  • Rojas C, Barnaeva E, Thomas AG, Hu X, Southall N, Marugan J, Chaudhuri AD, Yoo S-W, Hin N, Stepanek O (2018) DPTIP, a newly identified potent brain penetrant neutral sphingomyelinase 2 inhibitor, regulates astrocyte-peripheral immune communication following brain inflammation. Sci Rep 8(1):1–11

    Google Scholar 

  • Roy B, Ghose S, Biswas S (2021) Therapeutic strategies for miRNA delivery to reduce hepatocellular carcinoma. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2021.04.006

    Article  PubMed  Google Scholar 

  • Runz S, Keller S, Rupp C, Stoeck A, Issa Y, Koensgen D, Mustea A, Sehouli J, Kristiansen G, Altevogt P (2007) Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol 107(3):563–571

    CAS  PubMed  Google Scholar 

  • Rupert DL, Lässer C, Eldh M, Block S, Zhdanov VP, Lotvall JO, Bally M, Höök F (2014) Determination of exosome concentration in solution using surface plasmon resonance spectroscopy. Anal Chem 86(12):5929–5936

    CAS  PubMed  Google Scholar 

  • Ryu KJ, Lee JY, Park C, Cho D, Kim SJ (2020) Isolation of small extracellular vesicles from human serum using a combination of ultracentrifugation with polymer-based precipitation. Ann Lab Med 40:253–258

    CAS  PubMed  Google Scholar 

  • Sandfeld-Paulsen B, Jakobsen KR, Bæk R, Folkersen BH, Rasmussen TR, Meldgaard P, Varming K, Jørgensen MM, Sorensen BS (2016) Exosomal proteins as diagnostic biomarkers in lung cancer. J Thorac Oncol 11(10):1701–1710

    PubMed  Google Scholar 

  • Sargazi S, Ahmadi Z, Barani M, Rahdar A, Amani S, Desimone MF, Pandey S, Kyzas GZ (2022a) Can nanomaterials support the diagnosis and treatment of human infertility? A preliminary review. Life Sci 5:120539

    Google Scholar 

  • Sargazi S, Siddiqui B, Qindeel M, Rahdar A, Bilal M, Behzadmehr R, Mirinejad S, Pandey S (2022b) Chitosan nanocarriers for microRNA delivery and detection: a preliminary review with emphasis on cancer. Carbohydr Polym 290:119489

    CAS  PubMed  Google Scholar 

  • Sarkar C, Mondal M, Torequl Islam M, Martorell M, Docea AO, Maroyi A, Sharifi-Rad J, Calina D (2020) Potential therapeutic options for COVID-19: current status, challenges, and future perspectives. Front Pharmacol 11:572870

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sella A, Kilbourn R, Amato R, Bui C, Zukiwski AA, Ellerhorst J, Logothetis CJ (1994) Phase II study of ketoconazole combined with weekly doxorubicin in patients with androgen-independent prostate cancer. J Clin Oncol 12(4):683–688

    CAS  PubMed  Google Scholar 

  • Shahraki K, Ahani A, Sharma P, Faranoush M, Bahoush G, Torktaz I, Gahl W, Naseripour M, Behnam B (2017) Genetic screening in Iranian patients with retinoblastoma. Eye 31(4):620–627

    CAS  PubMed  Google Scholar 

  • Shi Z-Y, Yang X-X, Malichewe C, Li Y-S, Guo X-L (2020) Exosomal microRNAs-mediated intercellular communication and exosome-based cancer treatment. Int J Biol Macromol 158:530–541

    CAS  PubMed  Google Scholar 

  • Skotland T, Sandvig K, Llorente A (2017) Lipids in exosomes: current knowledge and the way forward. Prog Lipid Res 66:30–41

    CAS  PubMed  Google Scholar 

  • Sluijter JP, Verhage V, Deddens JC, van den Akker F, Doevendans PA (2014) Microvesicles and exosomes for intracardiac communication. Cardiovasc Res 102(2):302–311

    CAS  PubMed  Google Scholar 

  • Sohrabi B, Dayeri B, Zahedi E, Khoshbakht S, Nezamabadi Pour N, Ranjbar H, Davari Nejad A, Noureddini M, Alani B (2022) Mesenchymal stem cell (msc)-derived exosomes as novel vehicles for delivery of mirnas in cancer therapy. Cancer Gene Ther 29:1–12

    Google Scholar 

  • Spugnini EP, Logozzi M, Di Raimo R, Mizzoni D, Fais S (2018) A role of tumor-released exosomes in paracrine dissemination and metastasis. Int J Mol Sci 19(12):3968

    PubMed  PubMed Central  Google Scholar 

  • Stalder L, Heusermann W, Sokol L, Trojer D, Wirz J, Hean J, Fritzsche A, Aeschimann F, Pfanzagl V, Basselet P (2013) The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J 32(8):1115–1127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stolz A, Ernst A, Dikic I (2014) Cargo recognition and trafficking in selective autophagy. Nat Cell Biol 16(6):495–501

    CAS  PubMed  Google Scholar 

  • Sun D, Zhuang X, Xiang X, Liu Y, Zhang S, Liu C, Barnes S, Grizzle W, Miller D, Zhang H-G (2010) A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 18(9):1606–1614

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Kamohara H, Kinoshita K, Kurashige J, Ishimoto T, Iwatsuki M, Watanabe M, Baba H (2013) Clinical impact of serum exosomal microRNA-21 as a clinical biomarker in human esophageal squamous cell carcinoma. Cancer 119(6):1159–1167

    CAS  PubMed  Google Scholar 

  • Tatischeff I, Alfsen A (2011) A new biological strategy for drug delivery: eucaryotic cell-derived nanovesicles. J Biomater Nanobiotechnol 2(05):494

    CAS  Google Scholar 

  • Taylor S, Spugnini EP, Assaraf YG, Azzarito T, Rauch C, Fais S (2015) Microenvironment acidity as a major determinant of tumor chemoresistance: proton pump inhibitors (PPIs) as a novel therapeutic approach. Drug Resist Updat 23:69–78

    PubMed  Google Scholar 

  • Tkach M, Théry C (2016) Communication by extracellular vesicles: where we are and where we need to go. Cell 164(6):1226–1232

    CAS  PubMed  Google Scholar 

  • Urbanelli L, Magini A, Buratta S, Brozzi A, Sagini K, Polchi A, Tancini B, Emiliani C (2013) Signaling pathways in exosomes biogenesis, secretion and fate. Genes 4(2):152–170

    PubMed  PubMed Central  Google Scholar 

  • Van den Boorn JG, Schlee M, Coch C, Hartmann G (2011) SiRNA delivery with exosome nanoparticles. Nat Biotechnol 29(4):325–326

    PubMed  Google Scholar 

  • Verderio C, Gabrielli M, Giussani P (2018) Role of sphingolipids in the biogenesis and biological activity of extracellular vesicles. J Lipid Res 59(8):1325–1340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wahlgren J, Karlson TDL, Brisslert M, Vaziri Sani F, Telemo E, Sunnerhagen P, Valadi H (2012) Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 40(17):e130–e130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Hou L, Li A, Duan Y, Gao H, Song X (2014) Expression of serum exosomal microRNA-21 in human hepatocellular carcinoma. BioMed Res Int 2014:1–5

    Google Scholar 

  • Wang P, Wang H, Huang Q, Peng C, Yao L, Chen H, Qiu Z, Wu Y, Wang L, Chen W (2019a) Exosomes from M1-polarized macrophages enhance paclitaxel antitumor activity by activating macrophages-mediated inflammation. Theranostics 9(6):1714

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Chen L, Huang Y, Li K, Jinye A, Fan T, Zhao R, Xia X, Shen B, Du J (2019b) Exosome-delivered TRPP2 siRNA inhibits the epithelial-mesenchymal transition of FaDu cells. Oncol Lett 17(2):1953–1961

    CAS  PubMed  Google Scholar 

  • Wang H, He D, Wan K, Sheng X, Cheng H, Huang J, Zhou X, He X, Wang K (2020) In situ multiplex detection of serum exosomal microRNAs using an all-in-one biosensor for breast cancer diagnosis. Analyst 145(9):3289–3296

    CAS  PubMed  Google Scholar 

  • Whitford W, Guterstam P (2019) Exosome manufacturing status. Future Med Chem 11(10):1225–1236

    CAS  PubMed  Google Scholar 

  • Wilson K (2001) Preparation of genomic DNA from bacteria. Curr Protoc Mol Biol 56(1):2.4.1-2.4.5

    Google Scholar 

  • Yan S, Han B, Gao S, Wang X, Wang Z, Wang F, Zhang J, Xu D, Sun B (2017) Exosome-encapsulated microRNAs as circulating biomarkers for colorectal cancer. Oncotarget 8(36):60149

    PubMed  PubMed Central  Google Scholar 

  • Yang T, Martin P, Fogarty B, Brown A, Schurman K, Phipps R, Yin VP, Lockman P, Bai S (2015) Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm Res 32(6):2003–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Xie J, Zhu J, Kang C, Chiang C, Wang X, Wang X, Kuang T, Chen F, Chen Z (2016) Functional exosome-mimic for delivery of siRNA to cancer: in vitro and in vivo evaluation. J Control Release 243:160–171

    CAS  PubMed  Google Scholar 

  • Yang T, Fogarty B, LaForge B, Aziz S, Pham T, Lai L, Bai S (2017) Delivery of small interfering RNA to inhibit vascular endothelial growth factor in zebrafish using natural brain endothelia cell-secreted exosome nanovesicles for the treatment of brain cancer. AAPS J 19(2):475–486

    CAS  PubMed  Google Scholar 

  • Zaborowski MP, Balaj L, Breakefield XO, Lai CP (2015) Extracellular vesicles: composition, biological relevance, and methods of study. Bioscience 65(8):783–797

    PubMed  PubMed Central  Google Scholar 

  • Zakharova L, Svetlova M, Fomina AF (2007) T cell exosomes induce cholesterol accumulation in human monocytes via phosphatidylserine receptor. J Cell Physiol 212(1):174–181

    CAS  PubMed  Google Scholar 

  • Zhang T, Li Y, Yu Y, Zou P, Jiang Y, Sun D (2009) Characterization of celastrol to inhibit hsp90 and cdc37 interaction. J Biol Chem 284(51):35381–35389

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhang Y, Li Y (2013) β-elemene decreases cell invasion by upregulating E-cadherin expression in MCF-7 human breast cancer cells. Oncol Rep 30(2):745–750

    CAS  PubMed  Google Scholar 

  • Zhang J, Yao Y-F, Zhong S-L, Zhao JH, Tang JH (2015) β-elemene reverses chemoresistance of breast cancer cells by reducing resistance transmission via exosomes. Cell Physiol Biochem 36(6):2274–2286

    CAS  PubMed  Google Scholar 

  • Zhang J, Yan S, Yuan D, Alici G, Nguyen N-T, Warkiani ME, Li W (2016) Fundamentals and applications of inertial microfluidics: a review. Lab Chip 16(1):10–34

    CAS  PubMed  Google Scholar 

  • Zhang X, Zheng H, Wang Y (2017) Protective effects of catalpol exosomes on damaged SH-SY5Y cells induced by low serum medium. Global Tradit Chin Med 10(2):155–158

    Google Scholar 

  • Zhang Y, Liu Y, Liu H, Tang WH (2019) Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci 9(1):1–18

    Google Scholar 

  • Zhang Y, Bi J, Huang J, Tang Y, Du S, Li P (2020a) Exosome: a review of its classification, isolation techniques, storage, diagnostic and targeted therapy applications. Int J Nanomed 15:6917

    CAS  Google Scholar 

  • Zhang H, Lu J, Liu J, Zhang G, Lu A (2020b) Advances in the discovery of exosome inhibitors in cancer. J Enzyme Inhib Med Chem 35(1):1322–1330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Gu C, Gan Y, Shao L, Chen H, Zhu H (2020) Exosome-mediated siRNA delivery to suppress postoperative breast cancer metastasis. J Control Release 318:1–15

    CAS  PubMed  Google Scholar 

  • Zheng Z, Li Z, Xu C, Guo B, Guo P (2019) Folate-displaying exosome mediated cytosolic delivery of siRNA avoiding endosome trapping. J Control Release 311:43–49

    PubMed  Google Scholar 

  • Zhu L, Wang K, Cui J, Liu H, Bu X, Ma H, Wang W, Gong H, Lausted C, Hood L (2014) Label-free quantitative detection of tumor-derived exosomes through surface plasmon resonance imaging. Anal Chem 86(17):8857–8864

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zlotogorski-Hurvitz A, Dayan D, Chaushu G, Korvala J, Salo T, Sormunen R, Vered M (2015) Human saliva-derived exosomes: comparing methods of isolation. J Histochem Cytochem 63(3):181–189

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The authors have not disclosed any funding.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sakine Shirvalilou or Roghayeh Sheervalilou.

Ethics declarations

Conflict of interest

"The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article".

Consent to participate

“All authors participated in the investigation, design, interpretation of the studies and analysis of the data and review of the manuscript”.

Consent for publication

All authors are agreed.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shahraki, K., Boroumand, P.G., Lotfi, H. et al. An update in the applications of exosomes in cancer theranostics: from research to clinical trials. J Cancer Res Clin Oncol 149, 8087–8116 (2023). https://doi.org/10.1007/s00432-023-04701-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00432-023-04701-6

Keywords

Navigation