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Extracellular vesicle isolation, purification and evaluation in cancer diagnosis

Published online by Cambridge University Press:  21 October 2022

Keywan Mortezaee*
Affiliation:
Department of Anatomy, School of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran
Jamal Majidpoor
Affiliation:
Department of Anatomy, School of Medicine, Infectious Diseases Research Center, Gonabad University of Medical Sciences, Gonabad, Iran
Fardin Fathi*
Affiliation:
Department of Anatomy, School of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran
*
Authors for correspondence: Keywan Mortezaee, E-mail: [email protected]; Fardin Fathi, E-mail: [email protected]
Authors for correspondence: Keywan Mortezaee, E-mail: [email protected]; Fardin Fathi, E-mail: [email protected]

Abstract

Strategies for non-invasive biomarker discovery in early detection of cancer are an urgent need. Extracellular vesicles (EVs) have generated increasing attention from the scientific community and are under intensive investigations due to their unique biological profiles and their non-invasive nature. EVs are membrane-enclosed vesicles with variable sizes and function. Such vesicles are actively secreted from multiple cell types and are considered as key vehicles for inter-cellular communications and signalling. The stability and potential to easily cross biological barriers enable EVs for exerting durable effects on target cells. These along with easy access to such vesicles, the consistent secretion from tumour during all stages of tumorigenesis and their content providing a reservoir of molecules as well as mirroring the identity of the cell of origin are virtues that have made EVs appealing to be assessed in liquid biopsy approaches and for using as a promising resource of biomarkers in cancer diagnosis and therapy and monitoring targeted cancer therapy. Early detection of EVs will guide time-scheduled personalised therapy. Surveying reliable and sensitive methods for rapid isolation of EVs from biofluids, the purity of isolated vesicles and their molecular profiling and marker specification for clinical translation in patients with cancer are issues in the area and the hot topics of many recent studies. Here, the focus is over methods for EV isolation and stratification for digging more information about liquid biopsy-based diagnosis. Extending knowledge regarding EV-based strategies is a key to validate independent patient follow-up for cancer diagnosis at early stages and inspecting the efficacy of therapeutics.

Type
Review
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Kim, Y et al. (2016) Targeted proteomics identifies liquid-biopsy signatures for extracapsular prostate cancer. Nature Communications 7, 110.Google ScholarPubMed
Trinidad, CV et al. (2020) Reducing ovarian cancer mortality through early detection: approaches using circulating biomarkers. Cancer Prevention Research 13, 241252.CrossRefGoogle ScholarPubMed
Sun, N et al. (2020) Purification of HCC-specific extracellular vesicles on nanosubstrates for early HCC detection by digital scoring. Nature Communications 11, 112.Google ScholarPubMed
Liu, Y et al. (2020) Extracellular vesicle tetraspanin-8 level predicts distant metastasis in non–small cell lung cancer after concurrent chemoradiation. Science advances 6, eaaz6162.CrossRefGoogle ScholarPubMed
Bu, J et al. (2021) Tri-modal liquid biopsy: combinational analysis of circulating tumor cells, exosomes, and cell-free DNA using machine learning algorithm. Clinical and Translational Medicine 11. doi: 10.1002/ctm2.499.CrossRefGoogle ScholarPubMed
Wang, J et al. (2020) Tracking extracellular vesicle phenotypic changes enables treatment monitoring in melanoma. Science Advances 6, eaax3223.CrossRefGoogle ScholarPubMed
Balaj, L et al. (2011) Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nature Communications 2, 19.CrossRefGoogle ScholarPubMed
Probert, C et al. (2019) Communication of prostate cancer cells with bone cells via extracellular vesicle RNA; a potential mechanism of metastasis. Oncogene 38, 17511763.CrossRefGoogle ScholarPubMed
Bonsergent, E et al. (2021) Quantitative characterization of extracellular vesicle uptake and content delivery within mammalian cells. Nature Communications 12, 111.CrossRefGoogle ScholarPubMed
Kim, SY et al. (2019) High-fidelity probing of the structure and heterogeneity of extracellular vesicles by resonance-enhanced atomic force microscopy infrared spectroscopy. Nature Protocols 14, 576593.Google ScholarPubMed
Liu, C et al. (2019) Low-cost thermophoretic profiling of extracellular-vesicle surface proteins for the early detection and classification of cancers. Nature Biomedical Engineering 3, 183193.Google ScholarPubMed
Sun, L and Meckes, DG (2021) Multiplex protein profiling method for extracellular vesicle protein detection. Scientific Reports 11, 113.Google ScholarPubMed
Liang, K et al. (2017) Nanoplasmonic quantification of tumour-derived extracellular vesicles in plasma microsamples for diagnosis and treatment monitoring. Nature Biomedical Engineering 1, 111.CrossRefGoogle ScholarPubMed
Najafi, M et al. (2021) The current knowledge concerning solid cancer and therapy. Journal of Biochemical and Molecular Toxicology 35, e22900.CrossRefGoogle ScholarPubMed
Whiteside, TL (2020) Validation of plasma-derived small extracellular vesicles as cancer biomarkers. Nature Reviews Clinical Oncology 17, 719720.CrossRefGoogle ScholarPubMed
Hinger, SA et al. (2018) Diverse long RNAs are differentially sorted into extracellular vesicles secreted by colorectal cancer cells. Cell Reports 25, 715725, e4.CrossRefGoogle ScholarPubMed
Zomer, A et al. (2015) In vivo imaging reveals extracellular vesicle-mediated phenocopying of metastatic behavior. Cell 161, 10461057.CrossRefGoogle ScholarPubMed
Rontogianni, S et al. (2019) Proteomic profiling of extracellular vesicles allows for human breast cancer subtyping. Communications Biology 2, 113.CrossRefGoogle ScholarPubMed
Lee, J-H et al. (2020) Evidence for liver and peripheral immune cells secreting tumor-suppressive extracellular vesicles in melanoma patients. EBioMedicine 62, 103119.CrossRefGoogle ScholarPubMed
Tian, F et al. (2021) Protein analysis of extracellular vesicles to monitor and predict therapeutic response in metastatic breast cancer. Nature Communications 12, 113.CrossRefGoogle ScholarPubMed
Sass, D et al. (2021) Extracellular vesicle associated and soluble immune marker profiles of psychoneurological symptom clusters in men with prostate cancer: an exploratory study. Translational Psychiatry 11, 18.Google ScholarPubMed
Servage, KA et al. (2020) Proteomic profiling of small extracellular vesicles secreted by human pancreatic cancer cells implicated in cellular transformation. Scientific Reports 10, 113.CrossRefGoogle ScholarPubMed
Chen, F et al. (2019) Extracellular vesicle-packaged HIF-1α-stabilizing lncRNA from tumour-associated macrophages regulates aerobic glycolysis of breast cancer cells. Nature Cell Biology 21, 498510.CrossRefGoogle ScholarPubMed
Lopatina, T et al. (2020) Targeting IL-3Rα on tumor-derived endothelial cells blunts metastatic spread of triple-negative breast cancer via extracellular vesicle reprogramming. Oncogenesis 9, 114.CrossRefGoogle ScholarPubMed
Hinestrosa, JP et al. (2022) Early-stage multi-cancer detection using an extracellular vesicle protein-based blood test. Communications Medicine 2, 19.CrossRefGoogle ScholarPubMed
Ko, SY et al. (2019) Cancer-derived small extracellular vesicles promote angiogenesis by heparin-bound, bevacizumab-insensitive VEGF, independent of vesicle uptake. Communications Biology 2, 117.Google ScholarPubMed
Kowal, J et al. (2016) Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proceedings of the National Academy of Sciences 113, E968E977.Google ScholarPubMed
Feng, Q et al. (2017) A class of extracellular vesicles from breast cancer cells activates VEGF receptors and tumour angiogenesis. Nature Communications 8, 117.CrossRefGoogle ScholarPubMed
Crescitelli, R, Lässer, C and Lötvall, J (2021) Isolation and characterization of extracellular vesicle subpopulations from tissues. Nature Protocols 16, 15481580.CrossRefGoogle ScholarPubMed
DeRita, RM et al. (2019) Tumor-derived extracellular vesicles require β1 integrins to promote anchorage-independent growth. Iscience 14, 199209.CrossRefGoogle ScholarPubMed
Zeng, A et al. (2020) Glioblastoma-derived extracellular vesicles facilitate transformation of astrocytes via reprogramming oncogenic metabolism. Iscience 23, 101420.CrossRefGoogle ScholarPubMed
Yekula, A et al. (2020) Large and small extracellular vesicles released by glioma cells in vitro and in vivo. Journal of Extracellular Vesicles 9, 1689784.CrossRefGoogle ScholarPubMed
Vagner, T et al. (2018) Large extracellular vesicles carry most of the tumour DNA circulating in prostate cancer patient plasma. Journal of Extracellular Vesicles 7, 1505403.CrossRefGoogle ScholarPubMed
Kamerkar, S et al. (2017) Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature 546, 498503.CrossRefGoogle ScholarPubMed
Hagey, DW et al. (2021) Extracellular vesicles are the primary source of blood-borne tumour-derived mutant KRAS DNA early in pancreatic cancer. Journal of Extracellular Vesicles 10, e12142.CrossRefGoogle ScholarPubMed
Crescitelli, R et al. (2020) Subpopulations of extracellular vesicles from human metastatic melanoma tissue identified by quantitative proteomics after optimized isolation. Journal of Extracellular Vesicles 9, 1722433.CrossRefGoogle ScholarPubMed
Kanada, M et al. (2015) Differential fates of biomolecules delivered to target cells via extracellular vesicles. Proceedings of the National Academy of Sciences 112, E1433E1442.CrossRefGoogle ScholarPubMed
Meldolesi, J (2018) Exosomes and ectosomes in intercellular communication. Current Biology 28, R435R444.CrossRefGoogle ScholarPubMed
Fan, SJ et al. (2020) Glutamine deprivation alters the origin and function of cancer cell exosomes. The EMBO Journal 39, e103009.CrossRefGoogle ScholarPubMed
Sandim, V and Monteiro, RQ (2020) Extracellular vesicle fingerprinting: the next generation for cancer diagnosis? Signal Transduction and Targeted Therapy 5, 13.CrossRefGoogle ScholarPubMed
Hoshino, A et al. (2020) Extracellular vesicle and particle biomarkers define multiple human cancers. Cell 182, 10441061, e18.CrossRefGoogle ScholarPubMed
Garcia-Martin, R et al. (2022) Tissue differences in the exosomal/small extracellular vesicle proteome and their potential as indicators of altered tissue metabolism. Cell Reports 38, 110277.CrossRefGoogle ScholarPubMed
Dao, TNT et al. (2022) Chimeric nanocomposites for the rapid and simple isolation of urinary extracellular vesicles. Journal of Extracellular Vesicles 11, e12195.CrossRefGoogle ScholarPubMed
Pelissier Vatter, FA et al. (2021) Extracellular vesicle–and particle-mediated communication shapes innate and adaptive immune responses. Journal of Experimental Medicine 218, e20202579.CrossRefGoogle Scholar
Jang, M et al. (2019) Extracellular vesicle (EV)-polyphenol nanoaggregates for microRNA-based cancer diagnosis. NPG Asia Materials 11, 110.CrossRefGoogle Scholar
Mortezaee, K (2021) Enriched cancer stem cells, dense stroma, and cold immunity: interrelated events in pancreatic cancer. Journal of Biochemical and Molecular Toxicology 35, e22708.CrossRefGoogle ScholarPubMed
Wang, S et al. (2019) Proteomic analysis of urinary extracellular vesicles reveal biomarkers for neurologic disease. EBioMedicine 45, 351361.CrossRefGoogle ScholarPubMed
Yang, J et al. (2020) Brain tumor diagnostic model and dietary effect based on extracellular vesicle microbiome data in serum. Experimental & Molecular Medicine 52, 16021613.CrossRefGoogle ScholarPubMed
Muraoka, S et al. (2022) Comprehensive proteomic profiling of plasma and serum phosphatidylserine-positive extracellular vesicles reveals tissue-specific proteins. iScience 25, 104012.CrossRefGoogle ScholarPubMed
Chen, I-H et al. (2017) Phosphoproteins in extracellular vesicles as candidate markers for breast cancer. Proceedings of the National Academy of Sciences 114, 31753180.CrossRefGoogle ScholarPubMed
Shin, H-S et al. (2019) Alppl2 is a potential diagnostic biomarker for pancreatic cancer-derived extracellular vesicles. Molecular Therapy-Methods & Clinical Development 15, 204210.CrossRefGoogle ScholarPubMed
Sancho-Albero, M et al. (2019) Cancer-derived exosomes loaded with ultrathin palladium nanosheets for targeted bioorthogonal catalysis. Nature Catalysis 2, 864872.CrossRefGoogle ScholarPubMed
Ueta, E et al. (2021) Extracellular vesicle-shuttled miRNAs as a diagnostic and prognostic biomarker and their potential roles in gallbladder cancer patients. Scientific Reports 11, 113.CrossRefGoogle ScholarPubMed
Su, Y et al. (2021) Plasma extracellular vesicle long RNA profiles in the diagnosis and prediction of treatment response for breast cancer. NPJ Breast Cancer 7, 110.CrossRefGoogle ScholarPubMed
Zhang, P et al. (2020) Molecular and functional extracellular vesicle analysis using nanopatterned microchips monitors tumor progression and metastasis. Science Translational Medicine 12. doi: 10.1126/scitranslmed.aaz2878.CrossRefGoogle ScholarPubMed
Wendler, F, Stamp, GW and Giamas, G (2016) Tumor–stromal cell communication: small vesicles signal big changes. Trends in Cancer 2, 326329.CrossRefGoogle ScholarPubMed
Hu, J et al. (2017) A signal-amplifiable biochip quantifies extracellular vesicle-associated RNAs for early cancer detection. Nature Communications 8, 111.Google ScholarPubMed
Park, J et al. (2021) An integrated magneto-electrochemical device for the rapid profiling of tumour extracellular vesicles from blood plasma. Nature Biomedical Engineering 5, 678689.CrossRefGoogle ScholarPubMed
Zhang, H et al. (2018) Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nature Cell Biology 20, 332343.Google ScholarPubMed
Zhang, Y et al. (2021) The effect of extracellular vesicles on the regulation of mitochondria under hypoxia. Cell Death & Disease 12, 114.Google ScholarPubMed
Mortezaee, K and Majidpoor, J (2022) Im) maturity in tumor ecosystem. Frontiers in Oncology 11, 813897.CrossRefGoogle ScholarPubMed
Mortezaee, K and Majidpoor, J (2021) Key promoters of tumor hallmarks. International Journal of Clinical Oncology 27, 114.Google ScholarPubMed
Mortezaee, K and Majidpoor, J (2021) The impact of hypoxia on immune state in cancer. Life Sciences 286, 120057.CrossRefGoogle ScholarPubMed
Majidpoor, J and Mortezaee, K (2021) Angiogenesis as a hallmark of solid tumors-clinical perspectives. Cellular Oncology 44, 123.CrossRefGoogle ScholarPubMed
Cordonnier, M et al. (2020) Tracking the evolution of circulating exosomal-PD-L1 to monitor melanoma patients. Journal of Extracellular Vesicles 9, 1710899.CrossRefGoogle ScholarPubMed
Wang, J et al. (2020) Exosomal PD-L1 and N-cadherin predict pulmonary metastasis progression for osteosarcoma patients. Journal of Nanobiotechnology 18, 123.CrossRefGoogle ScholarPubMed
Dhondt, B et al. (2020) Unravelling the proteomic landscape of extracellular vesicles in prostate cancer by density-based fractionation of urine. Journal of Extracellular Vesicles 9, 1736935.CrossRefGoogle ScholarPubMed
Ramirez-Garrastacho, M et al. (2021) Extracellular vesicles as a source of prostate cancer biomarkers in liquid biopsies: a decade of research. British Journal of Cancer 126, 120.Google ScholarPubMed
Yasui, T et al. (2017) Unveiling massive numbers of cancer-related urinary-microRNA candidates via nanowires. Science Advances 3, e1701133.CrossRefGoogle ScholarPubMed
Jung, J-H et al. (2021) Dual size-exclusion chromatography for efficient isolation of extracellular vesicles from bone marrow derived human plasma. Scientific Reports 11, 19.Google ScholarPubMed
Ekström, K et al. (2022) Characterization of surface markers on extracellular vesicles isolated from lymphatic exudate from patients with breast cancer. BMC Cancer 22, 117.CrossRefGoogle ScholarPubMed
Tucci, M et al. (2018) Serum exosomes as predictors of clinical response to ipilimumab in metastatic melanoma. Oncoimmunology 7, e1387706.Google ScholarPubMed
Shephard, AP et al. (2021) Stroma-derived extracellular vesicle mRNA signatures inform histological nature of prostate cancer. Journal of Extracellular Vesicles 10, e12150.CrossRefGoogle ScholarPubMed
Theodoraki, M-N et al. (2018) Clinical significance of PD-L1 + exosomes in plasma of head and neck cancer patients. Clinical Cancer Research 24, 896905.CrossRefGoogle ScholarPubMed
Vonlaufen, A et al. (2001) Integrin αvβ3 expression in colon carcinoma correlates with survival. Modern Pathology 14, 11261132.CrossRefGoogle Scholar
Zhang, J et al. (2020) Localized fluorescent imaging of multiple proteins on individual extracellular vesicles using rolling circle amplification for cancer diagnosis. Journal of Extracellular Vesicles 10, e12025.CrossRefGoogle ScholarPubMed
Fathi, M et al. (2021) Single-cell cloning of breast cancer cells secreting specific subsets of extracellular vesicles. Cancers 13, 4397.CrossRefGoogle ScholarPubMed
Jing, X et al. (2018) CD24 Is a potential biomarker for prognosis in human breast carcinoma. Cellular Physiology and Biochemistry 48, 111119.CrossRefGoogle ScholarPubMed
Altevogt, P et al. (2021) Novel insights into the function of CD24: a driving force in cancer. International Journal of Cancer 148, 546559.CrossRefGoogle ScholarPubMed
Kang, YT et al. (2020) Dual-isolation and profiling of circulating tumor cells and cancer exosomes from blood samples with melanoma using immunoaffinity-based microfluidic interfaces. Advanced Science 7, 2001581.CrossRefGoogle ScholarPubMed
Shen, X et al. (2021) Exosome-mediated transfer of CD44 from high-metastatic ovarian cancer cells promotes migration and invasion of low-metastatic ovarian cancer cells. Journal of Ovarian Research 14, 111.CrossRefGoogle ScholarPubMed
Lane, R et al. (2019) Cell-derived extracellular vesicles can be used as a biomarker reservoir for glioblastoma tumor subtyping. Communications Biology 2, 112.CrossRefGoogle ScholarPubMed
Zeng, Q et al. (2012) CD146, an epithelial-mesenchymal transition inducer, is associated with triple-negative breast cancer. Proceedings of the National Academy of Sciences 109, 11271132.CrossRefGoogle ScholarPubMed
Bandini, E et al. (2021) Early detection and investigation of extracellular vesicles biomarkers in breast cancer. Frontiers in Molecular Biosciences 8. doi: 10.3389/fmolb.2021.732900.CrossRefGoogle ScholarPubMed
Porcelli, L et al. (2021) uPAR + extracellular vesicles: a robust biomarker of resistance to checkpoint inhibitor immunotherapy in metastatic melanoma patients. Journal for Immunotherapy of Cancer 9. doi: 10.1136/jitc-2021-002372.CrossRefGoogle ScholarPubMed
Peinado, H et al. (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nature Medicine 18, 883891.CrossRefGoogle Scholar
Pegoraro, A et al. (2021) P2X7 promotes metastatic spreading and triggers release of miRNA-containing exosomes and microvesicles from melanoma cells. Cell Death & Disease 12, 112.CrossRefGoogle ScholarPubMed
Pietrowska, M et al. (2021) Proteomic profile of melanoma cell-derived small extracellular vesicles in patients’ plasma: a potential correlate of melanoma progression. Journal of Extracellular Vesicles 10, e12063.CrossRefGoogle ScholarPubMed
Zhao, X et al. (2021) Analysis of the expression profile of serum exosomal lncRNA in breast cancer patients. Annals of Translational Medicine 9. doi: 10.21037/atm-21-3483.CrossRefGoogle ScholarPubMed
Sun, J et al. (2021) Exosome-derived ADAM17 promotes liver metastasis in colorectal cancer. Frontiers in Pharmacology 12. doi: 10.3389/fphar.2021.734351.CrossRefGoogle ScholarPubMed
Hu, C et al. (2021) Exosomal cripto-1 serves as a potential biomarker for perihilar cholangiocarcinoma. Frontiers in Oncology 11, 3144.Google ScholarPubMed
Jiang, Y et al. (2021) Exosomal long noncoding RNA HOXD-AS1 promotes prostate cancer metastasis via miR-361-5p/FOXM1 axis. Cell Death & Disease 12, 114.CrossRefGoogle ScholarPubMed
Li, Y et al. (2021) A novel urine exosomal lncRNA assay to improve the detection of prostate cancer at initial biopsy: a retrospective multicenter diagnostic feasibility study. Cancers 13, 4075.CrossRefGoogle ScholarPubMed
Skog, J et al. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nature Cell Biology 10, 14701476.CrossRefGoogle ScholarPubMed
Al-Nedawi, K et al. (2008) Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nature Cell Biology 10, 619624.CrossRefGoogle ScholarPubMed
Lai, CP et al. (2015) Visualization and tracking of tumour extracellular vesicle delivery and RNA translation using multiplexed reporters. Nature Communications 6, 112.CrossRefGoogle ScholarPubMed
Valadi, H et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology 9, 654659.CrossRefGoogle ScholarPubMed
Melo, SA et al. (2014) Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell 26, 707721.CrossRefGoogle ScholarPubMed
Squadrito, ML et al. (2014) Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Reports 8, 14321446.CrossRefGoogle ScholarPubMed
Liu, Z et al. (2021) Exosome-mediated miR-25/miR-203 as a potential biomarker for esophageal squamous cell carcinoma: improving early diagnosis and revealing malignancy. Translational Cancer Research 10, 51745182.CrossRefGoogle ScholarPubMed
Guo, S et al. (2005) Green tea polyphenol epigallocatechin-3 gallate (EGCG) affects gene expression of breast cancer cells transformed by the carcinogen 7, 12–dimethylbenz [a] anthracene. The Journal of Nutrition 135, 2978S2986S.CrossRefGoogle ScholarPubMed
Lim, J et al. (2022) Microfluidic device for one-step detection of breast cancer-derived exosomal mRNA in blood using signal-amplifiable 3D nanostructure. Biosensors and Bioelectronics 197, 113753.Google ScholarPubMed
Zhao, H et al. (2016) Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism. Elife 5, e10250.CrossRefGoogle ScholarPubMed
Zaborowski, MP et al. (2019) Methods for systematic identification of membrane proteins for specific capture of cancer-derived extracellular vesicles. Cell Reports 27, 255268, e6.CrossRefGoogle ScholarPubMed
Tan, X et al. (2021) Quantification and immunoprofiling of bladder cancer cell-derived extracellular vesicles with microfluidic chemiluminescent ELISA. Biosensors and Bioelectronics: X 8, 100066.CrossRefGoogle Scholar
Correll, VL et al. (2022) Optimization of small extracellular vesicle isolation from expressed prostatic secretions in urine for in-depth proteomic analysis. Journal of Extracellular Vesicles 11, e12184.CrossRefGoogle ScholarPubMed
Dou, R et al. (2021) EMT-cancer cells-derived exosomal miR-27b-3p promotes circulating tumour cells-mediated metastasis by modulating vascular permeability in colorectal cancer. Clinical and Translational Medicine 11, e595.CrossRefGoogle ScholarPubMed
Vinik, Y et al. (2020) Proteomic analysis of circulating extracellular vesicles identifies potential markers of breast cancer progression, recurrence, and response. Science Advances 6, eaba5714.CrossRefGoogle Scholar
Guan, S et al. (2020) Characterization of urinary exosomes purified with size exclusion chromatography and ultracentrifugation. Journal of Proteome Research 19, 22172225.CrossRefGoogle ScholarPubMed
Mol, EA et al. (2017) Higher functionality of extracellular vesicles isolated using size-exclusion chromatography compared to ultracentrifugation. Nanomedicine: Nanotechnology, Biology and Medicine 13, 20612065.CrossRefGoogle ScholarPubMed
Gámez-Valero, A et al. (2016) Size-exclusion chromatography-based isolation minimally alters extracellular vesicles’ characteristics compared to precipitating agents. Scientific Reports 6, 19.CrossRefGoogle ScholarPubMed
Karttunen, J et al. (2019) Precipitation-based extracellular vesicle isolation from rat plasma co-precipitate vesicle-free microRNAs. Journal of Extracellular Vesicles 8, 1555410.Google ScholarPubMed
Zhou, W (2018) Development of immunomagnetic droplet-based digital immuno-PCR for the quantification of prostate specific antigen. Analytical Methods 10, 36903695.CrossRefGoogle Scholar
Ko, J et al. (2020) Single extracellular vesicle protein analysis using immuno-droplet digital polymerase chain reaction amplification. Advanced biosystems 4, 1900307.Google ScholarPubMed
Im, H et al. (2014) Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor. Nature Biotechnology 32, 490495.CrossRefGoogle ScholarPubMed
Runz, S et al. (2007) Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecologic Oncology 107, 563571.CrossRefGoogle ScholarPubMed
Wu, X et al. (2020) Exosome-templated nanoplasmonics for multiparametric molecular profiling. Science Advances 6, eaba2556.CrossRefGoogle ScholarPubMed
Zhang, P et al. (2019) Ultrasensitive detection of circulating exosomes with a 3D-nanopatterned microfluidic chip. Nature Biomedical Engineering 3, 438451.CrossRefGoogle ScholarPubMed
Scaranti, M et al. (2020) Exploiting the folate receptor α in oncology. Nature Reviews Clinical Oncology 17, 349359.CrossRefGoogle ScholarPubMed
Shao, H et al. (2012) Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nature Medicine 18, 18351840.CrossRefGoogle ScholarPubMed
Wang, Z et al. (2020) Dual-selective magnetic analysis of extracellular vesicle glycans. Matter 2, 150166.CrossRefGoogle Scholar
Pan, S et al. (2021) Extracellular vesicle drug occupancy enables real-time monitoring of targeted cancer therapy. Nature Nanotechnology 16, 734742.CrossRefGoogle ScholarPubMed
Clark, RT (2015) Imaging flow cytometry enhances particle detection sensitivity for extracellular vesicle analysis. Nature Methods 12, iii.CrossRefGoogle Scholar
Tu, H et al. (2017) Concurrence of extracellular vesicle enrichment and metabolic switch visualized label-free in the tumor microenvironment. Science Advances 3, e1600675.Google ScholarPubMed
Mortezaee, K (2021) Redox tolerance and metabolic reprogramming in solid tumors. Cell Biology International 45, 273286.Google ScholarPubMed
Mortezaee, K and Majidpoor, J (2022) Dysregulated metabolism: a friend-to-foe skewer of macrophages. International Reviews of Immunology, 117.CrossRefGoogle ScholarPubMed
Majidpoor, J and Mortezaee, K (2021) Steps in metastasis: an updated review. Medical Oncology 38, 117.CrossRefGoogle Scholar
Mortezaee, K (2021) Organ tropism in solid tumor metastasis: an updated review. Future Oncology 17, 19431961.Google Scholar
Melo, SA et al. (2015) Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature 523, 177182.CrossRefGoogle ScholarPubMed
Esposito, CL et al. (2021) Identification of a novel RNA aptamer that selectively targets breast cancer exosomes. Molecular Therapy-Nucleic Acids 23, 982994.CrossRefGoogle ScholarPubMed
Moon, P-G et al. (2016) Identification of developmental endothelial locus-1 on circulating extracellular vesicles as a novel biomarker for early breast cancer detection. Clinical Cancer Research 22, 17571766.Google ScholarPubMed
McKiernan, J et al. (2018) A prospective adaptive utility trial to validate performance of a novel urine exosome gene expression assay to predict high-grade prostate cancer in patients with prostate-specific antigen 2–10 ng/ml at initial biopsy. European Urology 74, 731738.CrossRefGoogle Scholar
Rode, MP et al. (2021) miR-425-5p as an exosomal biomarker for metastatic prostate cancer. Cellular Signalling 87, 110113.CrossRefGoogle ScholarPubMed
Zhong, M-E et al. (2019) Serum extracellular vesicles contain SPARC and LRG1 as biomarkers of colon cancer and differ by tumour primary location. EBioMedicine 50, 211223.CrossRefGoogle ScholarPubMed
Gudbergsson, JM et al. (2019) Systematic review of targeted extracellular vesicles for drug delivery–considerations on methodological and biological heterogeneity. Journal of Controlled Release 306, 108120.CrossRefGoogle ScholarPubMed
Geeurickx, E et al. (2019) The generation and use of recombinant extracellular vesicles as biological reference material. Nature Communications 10, 112.CrossRefGoogle ScholarPubMed
Liu, X et al. (2021) Stimuli-mediated specific isolation of exosomes from blood plasma for high-throughput profiling of cancer biomarkers. Small Methods 6, 2101234.Google ScholarPubMed
Geeurickx, E et al. (2021) Recombinant extracellular vesicles as biological reference material for method development, data normalization and assessment of (pre-) analytical variables. Nature Protocols 16, 603633.Google ScholarPubMed