Profiling extracellular vesicle surface proteins with 10 µL peripheral plasma within 4 h.


Journal

Journal of extracellular vesicles
ISSN: 2001-3078
Titre abrégé: J Extracell Vesicles
Pays: United States
ID NLM: 101610479

Informations de publication

Date de publication:
09 2023
Historique:
revised: 19 07 2023
received: 01 03 2023
accepted: 22 08 2023
medline: 4 9 2023
pubmed: 1 9 2023
entrez: 1 9 2023
Statut: ppublish

Résumé

Extracellular vesicle (EV) surface proteins, expressed by primary tumours, are important biomarkers for early cancer diagnosis. However, the detection of these EV proteins is complicated by their low abundance and interference from non-EV components in clinical samples. Herein, we present a MEmbrane-Specific Separation and two-step Cascade AmpLificatioN (MESS2CAN) strategy for direct detection of EV surface proteins within 4 h. MESS2CAN utilises novel lipid probes (long chains linked by PEG2K with biotin at one end, and DSPE at the other end) and streptavidin-coated magnetic beads, permitting a 49.6% EV recovery rate within 1 h. A dual amplification strategy with a primer exchange reaction (PER) cascaded by the Cas12a system then allows sensitive detection of the target protein at 10 EV particles per microliter. Using 4 cell lines and 90 clinical test samples, we demonstrate MESS2CAN for analysing HER2, EpCAM and EGFR expression on EVs derived from cells and patient plasma. MESS2CAN reports the desired specificity and sensitivity of EGFR (AUC = 0.98) and of HER2 (AUC = 1) for discriminating between HER2-positive breast cancer, triple-negative breast cancer and healthy donors. MESS2CAN is a pioneering method for highly sensitive in vitro EV diagnostics, applicable to clinical samples with trace amounts of EVs.

Identifiants

pubmed: 37654045
doi: 10.1002/jev2.12364
pmc: PMC10471920
doi:

Substances chimiques

Membrane Proteins 0
Biotin 6SO6U10H04
ErbB Receptors EC 2.7.10.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e12364

Informations de copyright

© 2023 The Authors. Journal of Extracellular Vesicles published by Wiley Periodicals, LLC on behalf of the International Society for Extracellular Vesicles.

Références

Chen, J. S., Ma, E., Harrington, L. B., Da Costa, M., Tian, X., Palefsky, J. M., & Doudna, J. A. (2018). CRISPR-Cas12a target binding unleashes indiscriminate single-stranded DNase activity. Science, 360(6387), 436-439.
Chen, Y., Xue, F., Russo, A., & Wan, Y. (2021). Proteomic analysis of extracellular vesicles derived from MDA-MB-231 cells in microgravity. The Protein Journal, 40(1), 108-118.
Chen, Y., Zhu, Q., Cheng, L., Wang, Y., Li, M., Yang, Q., Hu, L., Lou, D., Li, J., Dong, X., Lee, L. P., & Liu, F. (2021). Exosome detection via the ultrafast-isolation system: EXODUS. Nature Methods, 18(2), 212-218.
Guo, Y., Tao, J., Li, Y., Feng, Y., Ju, H., Wang, Z., & Ding, L. (2020). Quantitative localized analysis reveals distinct exosomal protein-specific glycosignatures: Implications in cancer cell subtyping, exosome biogenesis, and function. Journal of the American Chemical Society, 142(16), 7404-7412.
He, F., Liu, H., Guo, X., Yin, B. C., & Ye, B. C. (2017). Direct exosome quantification via bivalent-cholesterol-labeled DNA anchor for signal amplification. Analytical Chemistry, 89(23), 12968-12975.
He, L., Yu, X., Huang, R., Jin, L., Liu, Y., Deng, Y., Li, S., Chen, H., Chen, Z., Li, Z., Xiao, P., & He, N. (2022). A novel specific and ultrasensitive method detecting extracellular vesicles secreted from lung cancer by padlock probe-based exponential rolling circle amplification. Nano Today, 42, 101334.
Im, H., Shao, H., Park, Y. I., Peterson, V. M., Castro, C. M., Weissleder, R., & Lee, H. (2014). Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor. Nature Biotechnology, 32(5), 490-495.
Ke, Y., Ghalandari, B., Huang, S., Li, S., Huang, C., Zhi, X., Cui, D., & Ding, X. (2022). 2'-O-Methyl modified guide RNA promotes the single nucleotide polymorphism (SNP) discrimination ability of CRISPR-Cas12a systems. Chemical Science, 13(7), 2050-2061.
Kilic, T., Cho, Y. K., Jeong, N., Shin, I.-S., Carter, B. S., Balaj, L., Weissleder, R., & Lee, H. (2022). Multielectrode spectroscopy enables rapid and sensitive molecular profiling of extracellular vesicles. ACS Central Science, 8(1), 110-117.
Kishi, J. Y., Lapan, S. W., Beliveau, B. J., West, E. R., Zhu, A., Sasaki, H. M., Saka, S. K., Wang, Y., Cepko, C. L., & Yin, P. (2019). SABER amplifies FISH: Enhanced multiplexed imaging of RNA and DNA in cells and tissues. Nature Methods, 16(6), 533-544.
Kishi, J. Y., Schaus, T. E., Gopalkrishnan, N., Xuan, F., & Yin, P. (2018). Programmable autonomous synthesis of single-stranded DNA. Nature Chemistry, 10(2), 155-164.
Kumar, P., Boyne, C., Brown, S., Qureshi, A., Thorpe, P., Synowsky, S. A., Shirran, S., & Powis, S. J. (2022). Tumour-associated antigenic peptides are present in the HLA class I ligandome of cancer cell line derived extracellular vesicles. Immunology, 166(2), 249-264.
Li, S., Zhu, Y., Haghniaz, R., Kawakita, S., Guan, S., Chen, J., Li, Z., Mandal, K., Bahari, J., Shah, S., Guo, J., Kang, H., Sun, W., Kim, H.-J., Jucaud, V., Dokmeci, M. R., Kollbaum, P., Lee, C. H., & Khademhosseini, A. (2022). A microchambers containing contact lens for the noninvasive detection of tear exosomes. Advanced Functional Materials, 32(44), 2206620.
Liang, K., Liu, F., Fan, J., Sun, D., Liu, C., Lyon, C. J., Bernard, D. W., Li, Y., Yokoi, K., Katz, M. H., Koay, E. J., Zhao, Z., & Hu, Y. (2017). Nanoplasmonic quantification of tumor-derived extracellular vesicles in plasma microsamples for diagnosis and treatment monitoring. Nature Biomedical Engineering, 1(4), 0021.
Liu, C., Zhao, J., Tian, F., Cai, L., Zhang, W., Feng, Q., Chang, J., Wan, F., Yang, Y., Dai, B., Cong, Y., Ding, B., Sun, J., & Tan, W. (2019). Low-cost thermophoretic profiling of extracellular-vesicle surface proteins for the early detection and classification of cancers. Nature Biomedical Engineering, 3(3), 183-193.
Mathieu, M., Martin-Jaular, L., Lavieu, G., & Thery, C. (2019). Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nature Cell Biology, 21(1), 9-17.
Melo, S. A., Luecke, L. B., Kahlert, C., Fernandez, A. F., Gammon, S. T., Kaye, J., LeBleu, V. S., Mittendorf, E. A., Weitz, J., Rahbari, N., Reissfelder, C., Pilarsky, C., Fraga, M. F., Piwnica-Worms, D., & Kalluri, R. (2015). Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature, 523(7559), 177-82.
Merchant, M. L., Rood, I. M., Deegens, J. K. J., & Klein, J. B. (2017). Isolation and characterization of urinary extracellular vesicles: implications for biomarker discovery. Nature Reviews Nephrology, 13(12), 731-749.
Mori, K., Hirase, M., Morishige, T., Takano, E., Sunayama, H., Kitayama, Y., Inubushi, S., Sasaki, R., Yashiro, M., & Takeuchi, T. (2019). A pretreatment-free, polymer-based platform prepared by molecular imprinting and post-imprinting modifications for sensing intact exosomes. Angewandte Chemie-International Edition, 58(6), 1612-1615.
Pan, W.-L., Feng, J.-J., Luo, T.-T., Tan, Y., Situ, B., Nieuwland, R., Guo, J.-Y., Liu, C.-C., Zhang, H., Chen, J., Zhang, W.-H., Chen, J., Chen, X.-H., Chen, H.-Y., Zheng, L., Chen, J.-X., & Li, B. (2022). Rapid and efficient isolation platform for plasma extracellular vesicles: EV-FISHER. Journal of Extracellular Vesicles, 11(11), e12281.
Park, J., Park, J. S., Huang, C.-H., Jo, A., Cook, K., Wang, R., Lin, H.-Y., Van Deun, J., Li, H., Min, J., Wang, L., Yoon, G., Carter, B. S., Balaj, L., Choi, G.-S., Castro, C. M., Weissleder, R., & Lee, H. (2021). An integrated magneto-electrochemical device for the rapid profiling of tumour extracellular vesicles from blood plasma. Nature Biomedical Engineering, 5(7), 678-689.
Piao, Y. J., Kim, H. S., Hwang, E. H., Woo, J., Zhang, M., & Moon, W. K. (2018). Breast cancer cell-derived exosomes and macrophage polarization are associated with lymph node metastasis. Oncotarget, 9(7), 7398-7410.
Qian, F., Huang, Z., Zhong, H., Lei, Q., Ai, Y., Xie, Z., Zhang, T., Jiang, B., Zhu, W., Sheng, Y., Hu, J., & Brinker, C. J. (2022). Analysis and biomedical applications of functional cargo in extracellular vesicles. ACS Nano, 16(12), 19980-20001.
Qingqing, Z., Ruigong, S., Jian-Ping, W., & Qi, Z. (2016). Influence of magnetic Fe3O4 nanoparticles on fluorescence quenching of dye molecules. Journal of Nanoscience and Nanotechnology, 16, 7432.
Rothlisberger, P., & Hollenstein, M. (2018). Aptamer chemistry. Advanced Drug Delivery Reviews, 134, 3-21.
Shao, H., Im, H., Castro, C. M., Breakefield, X., Weissleder, R., & Lee, H. (2018). New technologies for analysis of extracellular vesicles. Chemical Reviews, 118(4), 1917-1950.
Swarts, D. C., & Jinek, M. (2019). Mechanistic Insights into the cis- and trans-acting DNase activities of Cas12a. Molecular Cell, 73(3), 589-600e4.
van Niel, G., Carter, D. R. F., Clayton, A., Lambert, D. W., Raposo, G., & Vader, P. (2022). Challenges and directions in studying cell-cell communication by extracellular vesicles. Nature Reviews Molecular Cell Biology, 23(5), 369-382.
van Niel, G., D'Angelo, G., & Raposo, G. (2018). Shedding light on the cell biology of extracellular vesicles. Nature Reviews Molecular Cell Biology, 19(4), 213-228.
Wan, Y., Cheng, G., Liu, X., Hao, S.-J., Nisic, M., Zhu, C.-D., Xia, Y.-Q., Li, W.-Q., Wang, Z.-G., Zhang, W.-L., Rice, S. J., Sebastian, A., Albert, I., Belani, C. P., & Zheng, S.-Y. (2017). Rapid magnetic isolation of extracellular vesicles via lipid-based nanoprobes. Nature Biomedical Engineering, 1(4), 0058.
Wang, J., Wuethrich, A., Sina, A. A., Lane, R. E., Lin, L. L., Wang, Y., Cebon, J., Behren, A., & Trau, M. (2020). Tracking extracellular vesicle phenotypic changes enables treatment monitoring in melanoma. Science Advances, 6(9), eaax3223.
Wang, S., Zhang, L., Wan, S., Cansiz, S., Cui, C., Liu, Y., Cai, R., Hong, C., Teng, I. T., Shi, M., Wu, Y., Dong, Y., & Tan, W. (2017). Aptasensor with expanded nucleotide using DNA nanotetrahedra for electrochemical detection of cancerous exosomes. ACS Nano, 11(4), 3943-3949.
Witwer, K. W., Buzás, E. I., Bemis, L. T., Bora, A., Lässer, C., Lötvall, J., Nolte-‘t Hoen, E. N., Piper, M. G., Sivaraman, S., Skog, J., Théry, C., Wauben, M. H., & Hochberg, F. (2013). Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. Journal of Extracellular Vesicles, 2(1), 20360.
Xu, R., Rai, A., Chen, M., Suwakulsiri, W., Greening, D. W., & Simpson, R. J. (2018). Extracellular vesicles in cancer - implications for future improvements in cancer care. Nature Reviews Clinical Oncology, 15(10), 617-638.
Yan, S., Ahmad, K. Z., Li, S., Warden, A. R., Su, J., Zhang, Y., Yu, Y., Zhi, X., & Ding, X. (2021). Pre-coated interface proximity extension reaction assay enables trace protein detection with single-digit accuracy. Biosensors & Bioelectronics, 183, 113211.
Yildizhan, Y., Vajrala, V. S., Geeurickx, E., Declerck, C., Duskunovic, N., De Sutter, D., Noppen, S., Delport, F., Schols, D., Swinnen, J. V., Eyckerman, S., Hendrix, A., Lammertyn, J., & Spasic, D. (2021). FO-SPR biosensor calibrated with recombinant extracellular vesicles enables specific and sensitive detection directly in complex matrices. Journal of Extracellular Vesicles, 10(4), e12059.
Yu, D., Li, Y., Wang, M., Gu, J., Xu, W., Cai, H., Fang, X., & Zhang, X. (2022). Exosomes as a new frontier of cancer liquid biopsy. Molecular Cancer, 21(1), 56.
Zhang, B., Ma, W., Li, F., Gao, W., Zhao, Q., Peng, W., Piao, J., Wu, X., Wang, H., Gong, X., & Chang, J. (2017). Fluorescence quenching-based signal amplification on immunochromatography test strips for dual-mode sensing of two biomarkers of breast cancer. Nanoscale, 9(47), 18711-18722.

Auteurs

Jie He (J)

Department of Anesthesiology and Surgical Intensive Care Unit School of Medicine and School of Biomedical Engineering, Xinhua Hospital, Shanghai Jiao Tong University, Shanghai, China.
State Key Laboratory of Oncogenes and Related Genes, Institute for Personalized Medicine, Shanghai Jiao Tong University, Shanghai, China.

Hengyu Li (H)

Department of Breast and Thyroid Surgery, Changhai Hospital, Naval Military Medical University, Shanghai, China.

John Mai (J)

Alfred E. Mann Institute for Biomedical Engineering, University of Southern California, Los Angeles, California, USA.

Yuqing Ke (Y)

Department of Anesthesiology and Surgical Intensive Care Unit School of Medicine and School of Biomedical Engineering, Xinhua Hospital, Shanghai Jiao Tong University, Shanghai, China.
State Key Laboratory of Oncogenes and Related Genes, Institute for Personalized Medicine, Shanghai Jiao Tong University, Shanghai, China.

Chunhui Zhai (C)

Department of Anesthesiology and Surgical Intensive Care Unit School of Medicine and School of Biomedical Engineering, Xinhua Hospital, Shanghai Jiao Tong University, Shanghai, China.
State Key Laboratory of Oncogenes and Related Genes, Institute for Personalized Medicine, Shanghai Jiao Tong University, Shanghai, China.

Jiao Jiao Li (JJ)

School of Biomedical Engineering Faculty of Engineering and IT, University of Technology Sydney, Sydney, NSW, Australia.

Lai Jiang (L)

Department of Anesthesiology and Surgical Intensive Care Unit School of Medicine and School of Biomedical Engineering, Xinhua Hospital, Shanghai Jiao Tong University, Shanghai, China.
State Key Laboratory of Oncogenes and Related Genes, Institute for Personalized Medicine, Shanghai Jiao Tong University, Shanghai, China.

Guangxia Shen (G)

Department of Anesthesiology and Surgical Intensive Care Unit School of Medicine and School of Biomedical Engineering, Xinhua Hospital, Shanghai Jiao Tong University, Shanghai, China.
State Key Laboratory of Oncogenes and Related Genes, Institute for Personalized Medicine, Shanghai Jiao Tong University, Shanghai, China.

Xianting Ding (X)

Department of Anesthesiology and Surgical Intensive Care Unit School of Medicine and School of Biomedical Engineering, Xinhua Hospital, Shanghai Jiao Tong University, Shanghai, China.
State Key Laboratory of Oncogenes and Related Genes, Institute for Personalized Medicine, Shanghai Jiao Tong University, Shanghai, China.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH