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Biogenesis, Isolation, and Detection of Exosomes and Their Potential in Therapeutics and Diagnostics

Sonbhadra, Smrity, Mehak, Pandey, Lalit M.·2023·Biosensors
DOI 10.3390/bios13080802PMC PMC10452587
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Abstract

The increasing research and rapid developments in the field of exosomes provide insights into their role and significance in human health. Exosomes derived from various sources, such as mesenchymal stem cells, cardiac cells, and tumor cells, to name a few, can be potential therapeutic agents for the treatment of diseases and could also serve as biomarkers for the early detection of diseases. Cellular components of exosomes, several proteins, lipids, and miRNAs hold promise as novel biomarkers for the detection of various diseases. The structure of exosomes enables them as drug delivery vehicles. Since exosomes exhibit potential therapeutic applications, their efficient isolation from complex biological/clinical samples and precise real-time analysis becomes significant. With the advent of microfluidics, nano-biosensors are being designed to capture exosomes efficiently and rapidly. Herein, we have summarized the history, biogenesis, characteristics, functions, and applications of exosomes, along with the isolation, detection, and quantification techniques. The implications of surface modifications to enhance specificity have been outlined. The review also sheds light on the engineered nanoplatforms being developed for exosome detection and capture.

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Figure 2 (A) Biogenesis of exosomes showing their origin and release. Adapted from Liu et al., 2021 [46]. (B) Schematic representation of exosomal composition with its significant biomarkers. Adapted from Chen et al., 2022 [47].
Figure 2 (A) Biogenesis of exosomes showing their origin and release. Adapted from Liu et al., 2021 [46]. (B) Schematic representation of exosomal composition with its significant biomarkers. Adapted from Chen et al., 2022 [47].CC BY · PubMed Central
Figure 5 (A) Principle behind immunoaffinity-based method for isolating exosomes. Adapted and recreated from Yang et al., 2020 [64]. (B) Schematic diagram showing step-wise isolation of exosomes from MTEX by the capture of mAb 763.74 from bulk of non-aggregated exosomes. Adapted from Sharma et al., 2018 [82].
Figure 5 (A) Principle behind immunoaffinity-based method for isolating exosomes. Adapted and recreated from Yang et al., 2020 [64]. (B) Schematic diagram showing step-wise isolation of exosomes from MTEX by the capture of mAb 763.74 from bulk of non-aggregated exosomes. Adapted from Sharma et al., 2018 [82].CC BY · PubMed Central
Figure 1 Graphical abstract portraying the techniques involved in the isolation, detection, quantification, and characterization of exosomes.
Figure 1 Graphical abstract portraying the techniques involved in the isolation, detection, quantification, and characterization of exosomes.CC BY · PubMed Central
Figure 3 Step-wise isolation of exosomes using differential ultracentrifugation. Adapted from Yang et al., 2020 [64].
Figure 3 Step-wise isolation of exosomes using differential ultracentrifugation. Adapted from Yang et al., 2020 [64].CC BY · PubMed Central
Figure 4 (A) The average size of exosomes isolated from urine samples comparing three different modes of precipitation strategies. (B) Concentrations of isolated exosomes from urine (exosomes/mL). (C) Purity of the isolated exosome particles (exosome particles/µg protein from the urine sample). * p < 0.05, ** p < 0.01, *** p < 0.001, ns: no significance; n = 3. Adapted with permission from Cho et al., 2020 [76]. Copyright 2020 Elsevier.
Figure 4 (A) The average size of exosomes isolated from urine samples comparing three different modes of precipitation strategies. (B) Concentrations of isolated exosomes from urine (exosomes/mL). (C) Purity of the isolated exosome particles (exosome particles/µg protein from the urine sample). * p < 0.05, ** p < 0.01, *** p < 0.001, ns: no significance; n = 3. Adapted with permission from Cho et al., 2020 [76]. Copyright 2020 Elsevier.CC BY · PubMed Central
Figure 6 TEM images of exosomes isolated from three different cell lines (H3, BxPC3, and E10) using the ultrafiltration method, having molecular weight cut-off values of 30, 50, and 100 kDa. Scale bar: 200 nm. Adapted from Eduarda et al., 2018 [95].
Figure 6 TEM images of exosomes isolated from three different cell lines (H3, BxPC3, and E10) using the ultrafiltration method, having molecular weight cut-off values of 30, 50, and 100 kDa. Scale bar: 200 nm. Adapted from Eduarda et al., 2018 [95].CC BY · PubMed Central
Figure 7 Comparative efficiency of different techniques by measuring exosomal concentration (108/mL) of sample. Here, control is native cell culture supernatant; UF is ultrafiltration; UC is ultracentrifugation; and PT is precipitation. Adapted from Klymiuk et al., 2019 [96].
Figure 7 Comparative efficiency of different techniques by measuring exosomal concentration (108/mL) of sample. Here, control is native cell culture supernatant; UF is ultrafiltration; UC is ultracentrifugation; and PT is precipitation. Adapted from Klymiuk et al., 2019 [96].CC BY · PubMed Central
Figure 8 SEC—based isolation of exosomes from 1 mL of urine sample. (A) Y-axis shows exosome concentrations (particles/mL) and total protein concentrations in mg proteins/mL from all the collected SEC fractions. Bars represent exosome concentration and dotted line refers to protein concentration. (B) Average size of urinary exosomes isolated during SEC fractions 8–11. Adapted with permission from Cho et al., 2020 [76]. Copyright 2023 Elsevier.
Figure 8 SEC—based isolation of exosomes from 1 mL of urine sample. (A) Y-axis shows exosome concentrations (particles/mL) and total protein concentrations in mg proteins/mL from all the collected SEC fractions. Bars represent exosome concentration and dotted line refers to protein concentration. (B) Average size of urinary exosomes isolated during SEC fractions 8–11. Adapted with permission from Cho et al., 2020 [76]. Copyright 2023 Elsevier.CC BY · PubMed Central
Figure 9 Schematic diagram representing exosome detection using ECL biosensor-based in situ formation of AuNPs with Ti3C2 MXenes hybrid. (A) Shows the binding of aptamer (Apt) on MXenes hybrid surface. (B) The SA-PAM layer provides carboxyl groups for the immobilization of CD63 Apt molecules, which enables an efficient capturing of exosome molecules, followed by their detection using ECL biosensor. After the exosomes being captured, the exosomes/Apt/SA-PAM/GCE surfaces were incubated with the MXenes-Apt solution based on high specific binding between Apt and CD63 protein on exosomes surface. At last, the modified surfaces were immersed in HAuCl4 solution (2 mg/mL) forming a AuNPs-MXenes-Apt/exosomes/Apt/SA-PAM/GCE complex. The resulting ECL signal was recorded in luminol solution. [SA-PAM/GCE: Sodium alginate-poly(acrylamide)/glassy carbon electrode; MXenes: 2D inorganic compounds consisting of thin layers of transition metals]. Adapted with permission from Zhang et al., 2020 [123]. Copyright 2020 American Chemical Society.
Figure 9 Schematic diagram representing exosome detection using ECL biosensor-based in situ formation of AuNPs with Ti3C2 MXenes hybrid. (A) Shows the binding of aptamer (Apt) on MXenes hybrid surface. (B) The SA-PAM layer provides carboxyl groups for the immobilization of CD63 Apt molecules, which enables an efficient capturing of exosome molecules, followed by their detection using ECL biosensor. After the exosomes being captured, the exosomes/Apt/SA-PAM/GCE surfaces were incubated with the MXenes-Apt solution based on high specific binding between Apt and CD63 protein on exosomes surface. At last, the modified surfaces were immersed in HAuCl4 solution (2 mg/mL) forming a AuNPs-MXenes-Apt/exosomes/Apt/SA-PAM/GCE complex. The resulting ECL signal was recorded in luminol solution. [SA-PAM/GCE: Sodium alginate-poly(acrylamide)/glassy carbon electrode; MXenes: 2D inorganic compounds consisting of thin layers of transition metals]. Adapted with permission from Zhang et al., 2020 [123]. Copyright 2020 American Chemical Society.CC BY · PubMed Central
Figure 10 Working principle of SPRi biosensor for the detection of exosomes derived from NSCLC cells. AuNPs enhanced the signals. Adapted with permission from Fan et al., 2020 [149]. Copyright 2023 Elsevier.
Figure 10 Working principle of SPRi biosensor for the detection of exosomes derived from NSCLC cells. AuNPs enhanced the signals. Adapted with permission from Fan et al., 2020 [149]. Copyright 2023 Elsevier.CC BY · PubMed Central
Figure 11 Pie chart showing the types of lipid molecules (A) and phospholipids (B) associated with exosomes along with their percentage abundance in urine sample. For comparison, exosomes from PC-3 cell line have been shown. Adapted and recreated with permission from Skotland et al., 2017 [152]. Copyright 2023 Elsevier.
Figure 11 Pie chart showing the types of lipid molecules (A) and phospholipids (B) associated with exosomes along with their percentage abundance in urine sample. For comparison, exosomes from PC-3 cell line have been shown. Adapted and recreated with permission from Skotland et al., 2017 [152]. Copyright 2023 Elsevier.CC BY · PubMed Central
Figure 12 Detection of exosomes using iPM-based method. The bright spots represent the adsorption of exosomes onto positively charged surface, modified with gold. Scale bar: 5 µm. Adapted from Yang et al., 2018 [159].
Figure 12 Detection of exosomes using iPM-based method. The bright spots represent the adsorption of exosomes onto positively charged surface, modified with gold. Scale bar: 5 µm. Adapted from Yang et al., 2018 [159].CC BY · PubMed Central
Figure 13 (a) Schematic of isolation and magnetic separation of exosomes using CaTiO3:Eu3+@Fe3O4 nanocomposite. (b) SERS−based immune−assay for the detection of exosomes based on CD8. Adapted from Back et al., 2023 [169].
Figure 13 (a) Schematic of isolation and magnetic separation of exosomes using CaTiO3:Eu3+@Fe3O4 nanocomposite. (b) SERS−based immune−assay for the detection of exosomes based on CD8. Adapted from Back et al., 2023 [169].CC BY · PubMed Central
Figure 14 (a) Schematic of nanoplatform preparation and modification. (b) Illustration of exosome isolation and detection by the prepared Fe3O4@MgSiO3@CD63 nanoplatform. Adapted from Yang et al., 2021 [174].
Figure 14 (a) Schematic of nanoplatform preparation and modification. (b) Illustration of exosome isolation and detection by the prepared Fe3O4@MgSiO3@CD63 nanoplatform. Adapted from Yang et al., 2021 [174].CC BY · PubMed Central
Figure 15 The nanoplatform presented here consists of a silicon wafer shown in blue, onto which AuNPs are coated (yellow moieties). Further, PEG conjugation is done, represented by purple color. EDC/NHS reaction was carried out to activate PEG, as shown by green color. Exosomes from patient serum sample were immobilized onto the nanocomposite, as shown by oval shaped moieties. The schematic of the process depicts: (a) AuNP-coated Si- wafer. (b) PEG conjugation on AuNP-coated Si wafer. (c) EDC/NHS reaction for the activation of PEG. (d) Anti-CD63 antibody conjugation to Si wafer via PEG. (e) Immobilization of exosomes on the surface of Si wafer after incubation with patient serum sample. (f) Eluting exosomes from the surface of Si wafer. Adapted from Pammi et al., 2023 [175].
Figure 15 The nanoplatform presented here consists of a silicon wafer shown in blue, onto which AuNPs are coated (yellow moieties). Further, PEG conjugation is done, represented by purple color. EDC/NHS reaction was carried out to activate PEG, as shown by green color. Exosomes from patient serum sample were immobilized onto the nanocomposite, as shown by oval shaped moieties. The schematic of the process depicts: (a) AuNP-coated Si- wafer. (b) PEG conjugation on AuNP-coated Si wafer. (c) EDC/NHS reaction for the activation of PEG. (d) Anti-CD63 antibody conjugation to Si wafer via PEG. (e) Immobilization of exosomes on the surface of Si wafer after incubation with patient serum sample. (f) Eluting exosomes from the surface of Si wafer. Adapted from Pammi et al., 2023 [175].CC BY · PubMed Central
Figure 16 Various diseases for which exosomes act as therapeutic agents and biomarkers. Adapted from Rajput et al., 2022 [120].
Figure 16 Various diseases for which exosomes act as therapeutic agents and biomarkers. Adapted from Rajput et al., 2022 [120].CC BY · PubMed Central
Figure 17 The process of drug loading onto the exosomes and their infusion in patients. The various drugs/cargoes which can be loaded on exosomes are also shown. Adapted and recreated from Zhang et al., 2022 [207].
Figure 17 The process of drug loading onto the exosomes and their infusion in patients. The various drugs/cargoes which can be loaded on exosomes are also shown. Adapted and recreated from Zhang et al., 2022 [207].CC BY · PubMed Central

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Metadata

Authors
Sonbhadra, S., Mehak, & Pandey, L. M.
Affiliations
Bio-Interface & Environmental Engineering Lab, Department of Biosciences and Bioengineering, Indian Institute of Technology Guwahati, Assam 781039, India
Venue
Biosensors
Publisher
MDPI AG
Published
2023-08-10
Volume
13
Issue
8
Pages
802
ISSN
2079-6374
DOI
10.3390/bios13080802
PMC
PMC10452587
Cited by
97
References
9
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)

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