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Curated Papers > In recent years, high-impact research on "liquid biopsy" (IF≥30, past five years)

Exosome-based liquid biopsies in cancer: opportunities and challenges. ​

Literature Information ​

DOI10.1016/j.annonc.2021.01.074
PMID33548389
JournalAnnals of oncology : official journal of the European Society for Medical Oncology
Impact Factor65.4
JCR QuartileQ1
Publication Year2021
Times Cited413
Keywordscell-free DNA (cfDNA), circulating tumor DNA (ctDNA), circulating tumor cell (CTC), exosome, extracellular vesicle
Literature TypeJournal Article, Research Support, N.I.H., Extramural, Review
ISSN0923-7534
Pages466-477
Issue32(4)
AuthorsW Yu, J Hurley, D Roberts, S K Chakrabortty, D Enderle, M Noerholm, X O Breakefield, J K Skog

TL;DR ​

This review highlights the growing significance of exosomes and extracellular vesicles as a promising platform for liquid biopsy in cancer, offering potential advantages for early detection, treatment stratification, and monitoring disease recurrence. By containing tumor-derived materials and being stable in biofluids, exosome-based biomarkers are gaining traction in clinical applications, exemplified by their integration into guidelines for prostate cancer detection and their role in enhancing biomarker research.

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cell-free DNA (cfDNA) · circulating tumor DNA (ctDNA) · circulating tumor cell (CTC) · exosome · extracellular vesicle

Abstract ​

Liquid biopsy in cancer has gained momentum in clinical research and is experiencing a boom for a variety of applications. There are significant efforts to utilize liquid biopsies in cancer for early detection and treatment stratification, as well as residual disease and recurrence monitoring. Although most efforts have used circulating tumor cells and circulating tumor DNA for this purpose, exosomes and other extracellular vesicles have emerged as a platform with potentially broader and complementary applications. Exosomes/extracellular vesicles are small vesicles released by cells, including cancer cells, into the surrounding biofluids. These exosomes contain tumor-derived materials such as DNA, RNA, protein, lipid, sugar structures, and metabolites. In addition, exosomes carry molecules on their surface that provides clues regarding their origin, making it possible to sort vesicle types and enrich signatures from tissue-specific origins. Exosomes are part of the intercellular communication system and cancer cells frequently use them as biological messengers to benefit their growth. Since exosomes are part of the disease process, they have become of tremendous interest in biomarker research. Exosomes are remarkably stable in biofluids, such as plasma and urine, and can be isolated for clinical evaluation even in the early stages of the disease. Exosome-based biomarkers have quickly become adopted in the clinical arena and the first exosome RNA-based prostate cancer test has already helped >50 000 patients in their decision process and is now included in the National Comprehensive Cancer Network guidelines for early prostate cancer detection. This review will discuss the advantages and challenges of exosome-based liquid biopsies for tumor biomarkers and clinical implementation in the context of circulating tumor DNA and circulating tumor cells.

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Primary Questions Addressed ​

  1. What are the specific advantages of using exosome-based liquid biopsies compared to traditional methods like circulating tumor DNA and circulating tumor cells?
  2. How do exosomes enhance the understanding of tumor biology and intercellular communication in cancer progression?
  3. What are the current challenges faced in the clinical implementation of exosome-based biomarkers for cancer detection and monitoring?
  4. In what ways can exosome profiling contribute to personalized medicine approaches in oncology?
  5. What advancements in technology are necessary to improve the isolation and analysis of exosomes for clinical applications in cancer?

Key Findings ​

Research Background and Objectives ​

Liquid biopsies have emerged as a promising alternative to traditional tissue biopsies in cancer diagnostics, enabling less invasive, real-time insights into tumor biology. This review discusses the role of exosomes, a type of extracellular vesicle, in liquid biopsies, emphasizing their potential advantages over circulating tumor DNA (ctDNA) and circulating tumor cells (CTCs) for cancer detection and monitoring.

Main Methods/Materials/Experimental Design ​

The review focuses on the characterization and analysis of exosomes, their biological significance, and their application in liquid biopsies. The methodologies discussed include:

  • Exosome Isolation Techniques: Various methods to isolate exosomes from biofluids such as plasma, urine, and saliva, utilizing surface markers for enrichment.
  • Multi-analyte Approaches: Combining exosomal RNA with ctDNA and other biomarkers to enhance detection sensitivity and specificity.
  • Technological Advances: Development of novel assays and devices for the analysis of exosome-derived content, including RNA sequencing and microfluidic technologies.
Mermaid diagram

Key Results and Findings ​

  • Exosome Stability: Exosomes are stable in biofluids and can be isolated even in early disease stages, providing a reliable source of tumor-derived biomarkers.
  • Enhanced Sensitivity: Studies indicate that combining exosomal RNA with ctDNA significantly improves mutation detection sensitivity, with some studies showing up to tenfold increases in detectable mutations.
  • Clinical Utility: The first exosome RNA-based test for prostate cancer has been integrated into clinical guidelines, demonstrating the practical application of exosome analysis in patient management.

Main Conclusions/Significance/Innovativeness ​

Exosomes present a versatile platform for liquid biopsies, offering unique biomarker profiles that can enhance cancer detection and monitoring. Their ability to provide insights into the living tumor microenvironment makes them particularly valuable for early detection and treatment stratification. The review highlights the potential for exosome-based assays to revolutionize cancer diagnostics, moving beyond the limitations of traditional approaches.

Research Limitations and Future Directions ​

  • Technical Challenges: The enrichment and characterization of exosomes remain technically demanding, with issues related to surface marker specificity and the potential for nonspecific binding.
  • Need for Standardization: The variability in exosome isolation and analysis methods necessitates the development of standardized protocols to ensure reproducibility and clinical applicability.
  • Broader Applications: Future research should explore the application of exosome-based diagnostics beyond oncology, including neurodegenerative diseases and cardiovascular conditions.

Overall, the review underscores the transformative potential of exosome-based liquid biopsies in oncology, advocating for further research and technological advancements to fully realize their clinical utility.

References ​

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  2. Assessment of EGFR mutations in circulating tumor cell preparations from NSCLC patients by next generation sequencing: toward a real-time liquid biopsy for treatment. - Antonio Marchetti;Maela Del Grammastro;Lara Felicioni;Sara Malatesta;Giampaolo Filice;Irene Centi;Tommaso De Pas;Armando Santoro;Antonio Chella;Alba Ariela Brandes;Paola Venturino;Franco Cuccurullo;Lucio Crinò;Fiamma Buttitta - PloS one (2014)
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  6. Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. - Johann S de Bono;Howard I Scher;R Bruce Montgomery;Christopher Parker;M Craig Miller;Henk Tissing;Gerald V Doyle;Leon W W M Terstappen;Kenneth J Pienta;Derek Raghavan - Clinical cancer research : an official journal of the American Association for Cancer Research (2008)
  7. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. - Johan Skog;Tom Würdinger;Sjoerd van Rijn;Dimphna H Meijer;Laura Gainche;Miguel Sena-Esteves;William T Curry;Bob S Carter;Anna M Krichevsky;Xandra O Breakefield - Nature cell biology (2008)
  8. Molecular Detection and Analysis of Exosomes Using Surface-Enhanced Raman Scattering Gold Nanorods and a Miniaturized Device. - Elyahb Allie Kwizera;Ryan O'Connor;Vojtech Vinduska;Melody Williams;Elizabeth R Butch;Scott E Snyder;Xiang Chen;Xiaohua Huang - Theranostics (2018)
  9. Magnetic bead-based isolation of exosomes. - Morten P Oksvold;Axl Neurauter;Ketil W Pedersen - Methods in molecular biology (Clifton, N.J.) (2015)
  10. Urinary Exosomal and cell-free DNA Detects Somatic Mutation and Copy Number Alteration in Urothelial Carcinoma of Bladder. - Dong Hyeon Lee;Hana Yoon;Sanghui Park;Jeong Seon Kim;Young-Ho Ahn;Kihwan Kwon;Donghwan Lee;Kwang Hyun Kim - Scientific reports (2018)

Literatures Citing This Work ​

  1. EVs from BALF-Mediators of Inflammation and Potential Biomarkers in Lung Diseases. - Lukasz Zareba;Jacek Szymanski;Zuzanna Homoncik;Malgorzata Czystowska-Kuzmicz - International journal of molecular sciences (2021)
  2. Towards Novel Non-Invasive Colorectal Cancer Screening Methods: A Comprehensive Review. - Allegra Ferrari;Isabelle Neefs;Sarah Hoeck;Marc Peeters;Guido Van Hal - Cancers (2021)
  3. The Role of Extracellular Vesicles in the Progression of Human Neuroblastoma. - Danilo Marimpietri;Irma Airoldi;Angelo Corso Faini;Fabio Malavasi;Fabio Morandi - International journal of molecular sciences (2021)
  4. Liquid Biomarkers for Improved Diagnosis and Classification of CNS Tumors. - Severa Bunda;Jeffrey A Zuccato;Mathew R Voisin;Justin Z Wang;Farshad Nassiri;Vikas Patil;Sheila Mansouri;Gelareh Zadeh - International journal of molecular sciences (2021)
  5. The role and application of small extracellular vesicles in gastric cancer. - Hao Wu;Mengdi Fu;Jin Liu;Wei Chong;Zhen Fang;Fengying Du;Yang Liu;Liang Shang;Leping Li - Molecular cancer (2021)
  6. Circulating Exosomal MiR-107 Restrains Tumorigenesis in Diffuse Large B-Cell Lymphoma by Targeting 14-3-3η. - Jiarui Liu;Yang Han;Shunfeng Hu;Yiqing Cai;Juan Yang;Shuai Ren;Yi Zhao;Tiange Lu;Xiangxiang Zhou;Xin Wang - Frontiers in cell and developmental biology (2021)
  7. Exosome Traceability and Cell Source Dependence on Composition and Cell-Cell Cross Talk. - Rabab N Hamzah;Karrer M Alghazali;Alexandru S Biris;Robert J Griffin - International journal of molecular sciences (2021)
  8. Urine as a Source of Liquid Biopsy for Cancer. - Masanori Oshi;Vijayashree Murthy;Hideo Takahashi;Michelle Huyser;Maiko Okano;Yoshihisa Tokumaru;Omar M Rashid;Ryusei Matsuyama;Itaru Endo;Kazuaki Takabe - Cancers (2021)
  9. Identification of MicroRNAs as Viable Aggressiveness Biomarkers for Prostate Cancer. - Luis Javier Martínez-González;Victor Sánchez-Conde;Jose María González-Cabezuelo;Alba Antunez-Rodríguez;Eduardo Andrés-León;Inmaculada Robles-Fernandez;Jose Antonio Lorente;Fernando Vázquez-Alonso;María Jesus Alvarez-Cubero - Biomedicines (2021)
  10. Understanding the Pathophysiology of Exosomes in Schistosomiasis: A New Direction for Disease Control and Prevention. - Yue Yuan;Jianping Zhao;Min Chen;Huifang Liang;Xin Long;Bixiang Zhang;Xiaoping Chen;Qian Chen - Frontiers in immunology (2021)

... (403 more literatures)

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