Biosensor-based assay of exosome biomarker for early diagnosis of cancer

Ying Deng, Zhaowei Sun, Lei Wang, Minghui Wang, Jie Yang, Genxi Li

PDF(2667 KB)
PDF(2667 KB)
Front. Med. ›› 2022, Vol. 16 ›› Issue (2) : 157-175. DOI: 10.1007/s11684-021-0884-z
REVIEW
REVIEW

Biosensor-based assay of exosome biomarker for early diagnosis of cancer

Author information +
History +

Abstract

Cancer imposes a severe threat to people’s health and lives, thus pressing a huge medical and economic burden on individuals and communities. Therefore, early diagnosis of cancer is indispensable in the timely prevention and effective treatment for patients. Exosome has recently become an attractive cancer biomarker in noninvasive early diagnosis because of the unique physiology and pathology functions, which reflects remarkable information regarding the cancer microenvironment, and plays an important role in the occurrence and evolution of cancer. Meanwhile, biosensors have gained great attention for the detection of exosomes due to their superior properties, such as convenient operation, real-time readout, high sensitivity, and remarkable specificity, suggesting promising biomedical applications in the early diagnosis of cancer. In this review, the latest advances of biosensors regarding the assay of exosomes were summarized, and the superiorities of exosomes as markers for the early diagnosis of cancer were evaluated. Moreover, the recent challenges and further opportunities of developing effective biosensors for the early diagnosis of cancer were discussed.

Keywords

biosensor / exosome / cancer diagnosis

Cite this article

Download citation ▾
Ying Deng, Zhaowei Sun, Lei Wang, Minghui Wang, Jie Yang, Genxi Li. Biosensor-based assay of exosome biomarker for early diagnosis of cancer. Front. Med., 2022, 16(2): 157‒175 https://doi.org/10.1007/s11684-021-0884-z

References

[1]
Miller KD, Siegel RL, Lin CC, Mariotto AB, Kramer JL, Rowland JH, Stein KD, Alteri R, Jemal A. Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin 2016; 66(4): 271–289
CrossRef Pubmed Google scholar
[2]
Hou J, Li X, Xie KP. Coupled liquid biopsy and bioinformatics for pancreatic cancer early detection and precision prognostication. Mol Cancer 2021; 20(1): 34
CrossRef Pubmed Google scholar
[3]
Liu C, Yang Y, Wu Y. Recent advances in exosomal protein detection via liquid biopsy biosensors for cancer screening, diagnosis, and prognosis. AAPS J 2018; 20(2): 41
CrossRef Pubmed Google scholar
[4]
Siravegna G, Marsoni S, Siena S, Bardelli A. Integrating liquid biopsies into the management of cancer. Nat Rev Clin Oncol 2017; 14(9): 531–548
CrossRef Pubmed Google scholar
[5]
Soda N, Rehm BHA, Sonar P, Nguyen NT, Shiddiky MJA. Advanced liquid biopsy technologies for circulating biomarker detection. J Mater Chem B Mater Biol Med 2019; 7(43): 6670–6704
CrossRef Pubmed Google scholar
[6]
Zhang L, Gu C, Wen J, Liu G, Liu H, Li L. Recent advances in nanomaterial-based biosensors for the detection of exosomes. Anal Bioanal Chem 2021; 413(1): 83–102
CrossRef Pubmed Google scholar
[7]
LeBleu VS, Kalluri R. Exosomes as a multicomponent biomarker platform in cancer. Trends Cancer 2020; 6(9): 767–774
CrossRef Pubmed Google scholar
[8]
Sharma A, Johnson A. Exosome DNA: critical regulator of tumor immunity and a diagnostic biomarker. J Cell Physiol 2020; 235(3): 1921–1932
CrossRef Pubmed Google scholar
[9]
Skotland T, Sagini K, Sandvig K, Llorente A. An emerging focus on lipids in extracellular vesicles. Adv Drug Deliv Rev 2020; 159: 308–321
CrossRef Pubmed Google scholar
[10]
Sandfeld-Paulsen B, Aggerholm-Pedersen N, Bæk R, Jakobsen KR, Meldgaard P, Folkersen BH, Rasmussen TR, Varming K, Jørgensen MM, Sorensen BS. Exosomal proteins as prognostic biomarkers in non-small cell lung cancer. Mol Oncol 2016; 10(10): 1595–1602
CrossRef Pubmed Google scholar
[11]
Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014; 30(1): 255–289
CrossRef Pubmed Google scholar
[12]
Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science 2020; 367(6478): eaau6977
CrossRef Pubmed Google scholar
[13]
Maacha S, Bhat AA, Jimenez L, Raza A, Haris M, Uddin S, Grivel JC. Extracellular vesicles-mediated intercellular communication: roles in the tumor microenvironment and anti-cancer drug resistance. Mol Cancer 2019; 18(1): 55
CrossRef Pubmed Google scholar
[14]
Meldolesi J. Exosomes and ectosomes in intercellular communication. Curr Biol 2018; 28(8): R435–R444
CrossRef Pubmed Google scholar
[15]
Quek C, Hill AF. The role of extracellular vesicles in neurodegenerative diseases. Biochem Biophys Res Commun 2017; 483(4): 1178–1186
CrossRef Pubmed Google scholar
[16]
Silva J, Garcia V, Rodriguez M, Compte M, Cisneros E, Veguillas P, Garcia JM, Dominguez G, Campos-Martin Y, Cuevas J, Peña C, Herrera M, Diaz R, Mohammed N, Bonilla F. Analysis of exosome release and its prognostic value in human colorectal cancer. Genes Chromosomes Cancer 2012; 51(4): 409–418
CrossRef Pubmed Google scholar
[17]
Yu W, Hurley J, Roberts D, Chakrabortty SK, Enderle D, Noerholm M, Breakefield XO, Skog JK. Exosome-based liquid biopsies in cancer: opportunities and challenges. Ann Oncol 2021; 32(4): 466–477
CrossRef Pubmed Google scholar
[18]
Khodashenas S, Khalili S, Forouzandeh Moghadam M. A cell ELISA based method for exosome detection in diagnostic and therapeutic applications. Biotechnol Lett 2019; 41(4–5): 523–531
CrossRef Pubmed Google scholar
[19]
Dragovic RA, Collett GP, Hole P, Ferguson DJ, Redman CW, Sargent IL, Tannetta DS. Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence nanoparticle tracking analysis. Methods 2015; 87: 64–74
CrossRef Pubmed Google scholar
[20]
Chia BS, Low YP, Wang Q, Li P, Gao Z. Advances in exosome quantification techniques. Trends Analyt Chem 2017; 86: 93–106
CrossRef Google scholar
[21]
Mastoridis S, Bertolino GM, Whitehouse G, Dazzi F, Sanchez-Fueyo A, Martinez-Llordella M. Multiparametric analysis of circulating exosomes and other small extracellular vesicles by advanced imaging flow cytometry. Front Immunol 2018; 9: 1583
CrossRef Pubmed Google scholar
[22]
Luo X, An M, Cuneo KC, Lubman DM, Li L. High-performance chemical isotope labeling liquid chromatography mass spectrometry for exosome metabolomics. Anal Chem 2018; 90(14): 8314–8319
CrossRef Pubmed Google scholar
[23]
Ko J, Carpenter E, Issadore D. Detection and isolation of circulating exosomes and microvesicles for cancer monitoring and diagnostics using micro-/nano-based devices. Analyst (Lond) 2016; 141(2): 450–460
CrossRef Pubmed Google scholar
[24]
Witwer KW, Buzás EI, Bemis LT, Bora A, Lässer C, Lötvall J, Nolte-’t Hoen EN, Piper MG, Sivaraman S, Skog J, Théry C, Wauben MH, Hochberg F. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013; 2: 20360
CrossRef Pubmed Google scholar
[25]
Sun Z, Wang L, Wu S, Pan Y, Dong Y, Zhu S, Yang J, Yin Y, Li G. An electrochemical biosensor designed by using Zr-based metal-organic frameworks for the detection of glioblastoma-derived exosomes with practical application. Anal Chem 2020; 92(5): 3819–3826
CrossRef Pubmed Google scholar
[26]
Wang L, Pan Y, Liu Y, Sun Z, Huang Y, Li J, Yang J, Xiang Y, Li G. Fabrication of an aptamer-coated liposome complex for the detection and profiling of exosomes based on terminal deoxynucleotidyl transferase-mediated signal amplification. ACS Appl Mater Interfaces 2020; 12(1): 322–329
CrossRef Pubmed Google scholar
[27]
van der Pol E, Coumans F A W, Grootemaat AE, Gardiner C, Sargent IL, Harrison P, Sturk A, van Leeuwen TG, Nieuwland R. Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost 2014; 12(7): 1182–1192
CrossRef Pubmed Google scholar
[28]
Lin S, Yu Z, Chen D, Wang Z, Miao J, Li Q, Zhang D, Song J, Cui D. Progress in microfluidics-based exosome separation and detection technologies for diagnostic applications. Small 2020; 16(9): e1903916
CrossRef Pubmed Google scholar
[29]
Yoo SM, Lee SY. Optical biosensors for the detection of pathogenic microorganisms. Trends Biotechnol 2016; 34(1): 7–25
CrossRef Pubmed Google scholar
[30]
Masud MK, Na J, Younus M, Hossain MSA, Bando Y, Shiddiky MJA, Yamauchi Y. Superparamagnetic nanoarchitectures for disease-specific biomarker detection. Chem Soc Rev 2019; 48(24): 5717–5751
CrossRef Pubmed Google scholar
[31]
Huang Y, Wang L, Sha L, Wang Y, Duan X, Li G. Highly sensitive detection of lipopolysaccharide based on collaborative amplification of dual enzymes. Anal Chim Acta 2020; 1126: 31–37
CrossRef Pubmed Google scholar
[32]
Geng Y, Peveler WJ, Rotello VM. Array-based “chemical nose” sensing in diagnostics and drug discovery. Angew Chem Int Ed Engl 2019; 58(16): 5190–5200
CrossRef Pubmed Google scholar
[33]
Wu J, Hu S, Zhang L, Xin J, Sun C, Wang L, Ding K, Wang B. Tumor circulome in the liquid biopsies for cancer diagnosis and prognosis. Theranostics 2020; 10(10): 4544–4556
CrossRef Pubmed Google scholar
[34]
Guo SC, Tao SC, Dawn H. Microfluidics-based on-a-chip systems for isolating and analysing extracellular vesicles. J Extracell Vesicles 2018; 7(1): 1508271
CrossRef Pubmed Google scholar
[35]
Cheng N, Du D, Wang X, Liu D, Xu W, Luo Y, Lin Y. Recent advances in biosensors for detecting cancer-derived exosomes. Trends Biotechnol 2019; 37(11): 1236–1254
CrossRef Pubmed Google scholar
[36]
Wen W, Yan X, Zhu C, Du D, Lin Y. Recent advances in electrochemical immunosensors. Anal Chem 2017; 89(1): 138–156
CrossRef Pubmed Google scholar
[37]
Ogino S, Nowak JA, Hamada T Jr, Milner DA Jr, Nishihara R. Insights into pathogenic interactions among environment, host, and tumor at the crossroads of molecular pathology and epidemiology. Annu Rev Pathol 2019; 14(1): 83–103
CrossRef Pubmed Google scholar
[38]
Zhang L, Gu C, Wen J, Liu G, Liu H, Li L. Recent advances in nanomaterial-based biosensors for the detection of exosomes. Anal Bioanal Chem 2021; 413(1): 83–102
CrossRef Pubmed Google scholar
[39]
Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, Skog J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011; 2(1): 180
CrossRef Pubmed Google scholar
[40]
Mathieu M, Martin-Jaular L, Lavieu G, Théry C. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat Cell Biol 2019; 21(1): 9–17
CrossRef Pubmed Google scholar
[41]
Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967; 13(3): 269–288
CrossRef Pubmed Google scholar
[42]
Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987; 262(19): 9412–9420
CrossRef Pubmed Google scholar
[43]
Kowal J, Tkach M, Théry C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol 2014; 29: 116–125
CrossRef Pubmed Google scholar
[44]
Foster BP, Balassa T, Benen TD, Dominovic M, Elmadjian GK, Florova V, Fransolet MD, Kestlerova A, Kmiecik G, Kostadinova IA, Kyvelidou C, Meggyes M, Mincheva MN, Moro L, Pastuschek J, Spoldi V, Wandernoth P, Weber M, Toth B, Markert UR. Extracellular vesicles in blood, milk and body fluids of the female and male urogenital tract and with special regard to reproduction. Crit Rev Clin Lab Sci 2016; 53(6): 379–395
CrossRef Pubmed Google scholar
[45]
Delorme-Axford E, Donker RB, Mouillet JF, Chu T, Bayer A, Ouyang Y, Wang T, Stolz DB, Sarkar SN, Morelli AE, Sadovsky Y, Coyne CB. Human placental trophoblasts confer viral resistance to recipient cells. Proc Natl Acad Sci USA 2013; 110(29): 12048–12053
CrossRef Pubmed Google scholar
[46]
Gehrmann U, Näslund TI, Hiltbrunner S, Larssen P, Gabrielsson S. Harnessing the exosome-induced immune response for cancer immunotherapy. Semin Cancer Biol 2014; 28: 58–67
CrossRef Pubmed Google scholar
[47]
Cheng Y, Schorey JS. Extracellular vesicles deliver Mycobacterium RNA to promote host immunity and bacterial killing. EMBO Rep 2019; 20(3): e46613
CrossRef Pubmed Google scholar
[48]
de Carvalho JV, de Castro RO, da Silva EZ, Silveira PP, da Silva-Januário ME, Arruda E, Jamur MC, Oliver C, Aguiar RS, daSilva LL. Nef neutralizes the ability of exosomes from CD4+ T cells to act as decoys during HIV-1 infection. PLoS One 2014; 9(11): e113691
CrossRef Pubmed Google scholar
[49]
Guay C, Regazzi R. Exosomes as new players in metabolic organ cross-talk. Diabetes Obes Metab 2017; 19(Suppl 1): 137–146
CrossRef Pubmed Google scholar
[50]
Zhang Y, Hu YW, Zheng L, Wang Q. Characteristics and roles of exosomes in cardiovascular disease. DNA Cell Biol 2017; 36(3): 202–211
CrossRef Pubmed Google scholar
[51]
Budnik V, Ruiz-Cañada C, Wendler F. Extracellular vesicles round off communication in the nervous system. Nat Rev Neurosci 2016; 17(3): 160–172
CrossRef Pubmed Google scholar
[52]
Sundararajan V, Sarkar FH, Ramasamy TS. The multifaceted role of exosomes in cancer progression: diagnostic and therapeutic implications [corrected]. Cell Oncol (Dordr) 2018; 41(3): 223–252
CrossRef Pubmed Google scholar
[53]
Yang Y, Li CW, Chan LC, Wei Y, Hsu JM, Xia W, Cha JH, Hou J, Hsu JL, Sun L, Hung MC. Exosomal PD-L1 harbors active defense function to suppress T cell killing of breast cancer cells and promote tumor growth. Cell Res 2018; 28(8): 862–864
CrossRef Pubmed Google scholar
[54]
Fang T, Lv H, Lv G, Li T, Wang C, Han Q, Yu L, Su B, Guo L, Huang S, Cao D, Tang L, Tang S, Wu M, Yang W, Wang H. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun 2018; 9(1): 191
CrossRef Pubmed Google scholar
[55]
Liu X, Lu Y, Xu Y, Hou S, Huang J, Wang B, Zhao J, Xia S, Fan S, Yu X, Du Y, Hou L, Li Z, Ding Z, An S, Huang B, Li L, Tang J, Ju J, Guan H, Song B. Exosomal transfer of miR-501 confers doxorubicin resistance and tumorigenesis via targeting of BLID in gastric cancer. Cancer Lett 2019; 459: 122–134
CrossRef Pubmed Google scholar
[56]
Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, Rak J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008; 10(5): 619–624
CrossRef Pubmed Google scholar
[57]
Jakobsen KR, Paulsen BS, Bæk R, Varming K, Sorensen BS, Jørgensen MM. Exosomal proteins as potential diagnostic markers in advanced non-small cell lung carcinoma. J Extracell Vesicles 2015; 4(1): 26659
CrossRef Pubmed Google scholar
[58]
Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, LeBleu VS, Mittendorf EA, Weitz J, Rahbari N, Reissfelder C, Pilarsky C, Fraga MF, Piwnica-Worms D, Kalluri R. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature 2015; 523(7559): 177–182
CrossRef Pubmed Google scholar
[59]
Yoon JH, Ham IH, Kim O, Ashktorab H, Smoot DT, Nam SW, Lee JY, Hur H, Park WS. Gastrokine 1 protein is a potential theragnostic target for gastric cancer. Gastric Cancer 2018; 21(6): 956–967
CrossRef Pubmed Google scholar
[60]
Khan S, Bennit HF, Turay D, Perez M, Mirshahidi S, Yuan Y, Wall NR. Early diagnostic value of survivin and its alternative splice variants in breast cancer. BMC Cancer 2014; 14(1): 176
CrossRef Pubmed Google scholar
[61]
Zhang P, Zhou X, He M, Shang Y, Tetlow AL, Godwin AK, Zeng Y. Ultrasensitive detection of circulating exosomes with a 3D-nanopatterned microfluidic chip. Nat Biomed Eng 2019; 3(6): 438–451
CrossRef Pubmed Google scholar
[62]
Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O’Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105(30): 10513–10518
CrossRef Pubmed Google scholar
[63]
Sun Z, Shi K, Yang S, Liu J, Zhou Q, Wang G, Song J, Li Z, Zhang Z, Yuan W. Effect of exosomal miRNA on cancer biology and clinical applications. Mol Cancer 2018; 17(1): 147
CrossRef Pubmed Google scholar
[64]
Li Z, Ma YY, Wang J, Zeng XF, Li R, Kang W, Hao XK. Exosomal microRNA-141 is upregulated in the serum of prostate cancer patients. Onco Targets Ther 2015; 9: 139–148
Pubmed
[65]
Zhou CF, Ma J, Huang L, Yi HY, Zhang YM, Wu XG, Yan RM, Liang L, Zhong M, Yu YH, Wu S, Wang W. Cervical squamous cell carcinoma-secreted exosomal miR-221-3p promotes lymphangiogenesis and lymphatic metastasis by targeting VASH1. Oncogene 2019; 38(8): 1256–1268
CrossRef Pubmed Google scholar
[66]
Wang X, Luo G, Zhang K, Cao J, Huang C, Jiang T, Liu B, Su L, Qiu Z. Hypoxic tumor-derived exosomal miR-301a mediates M2 macrophage polarization via PTEN/PI3Kγ to promote pancreatic cancer metastasis. Cancer Res 2018; 78(16): 4586–4598 doi:10.1158/0008-5472.CAN-17-3841
Pubmed
[67]
Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144(5): 646–674
CrossRef Pubmed Google scholar
[68]
Boriachek K, Umer M, Islam MN, Gopalan V, Lam AK, Nguyen NT, Shiddiky MJA. An amplification-free electrochemical detection of exosomal miRNA-21 in serum samples. Analyst (Lond) 2018; 143(7): 1662–1669
CrossRef Pubmed Google scholar
[69]
Li Y, Zhang Y, Qiu F, Qiu Z. Proteomic identification of exosomal LRG1: a potential urinary biomarker for detecting NSCLC. Electrophoresis 2011; 32(15): 1976–1983
CrossRef Pubmed Google scholar
[70]
Kim HK, Jeong H, Choi BH, Quan YH, Rho J, Park JH, Park Y, Choi Y, Han KN, Choi YH, Hong S. Lung cancer exosome specific protein 1 (LESP-1) as a potential factor for diagnosis and treatment of non-small cell lung cancer. J Clin Oncol 2020; 38(15_suppl): e15550
CrossRef Google scholar
[71]
Tian Y, Ma L, Gong M, Su G, Zhu S, Zhang W, Wang S, Li Z, Chen C, Li L, Wu L, Yan X. Protein profiling and sizing of extracellular vesicles from colorectal cancer patients via flow cytometry. ACS Nano 2018; 12(1): 671–680
CrossRef Pubmed Google scholar
[72]
Khan S, Bennit HF, Turay D, Perez M, Mirshahidi S, Yuan Y, Wall NR. Early diagnostic value of survivin and its alternative splice variants in breast cancer. BMC Cancer 2014; 14(1): 176
CrossRef Pubmed Google scholar
[73]
Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008; 110(1): 13–21
CrossRef Pubmed Google scholar
[74]
Zhou X, Wen W, Shan X, Zhu W, Xu J, Guo R, Cheng W, Wang F, Qi LW, Chen Y, Huang Z, Wang T, Zhu D, Liu P, Shu Y. A six-microRNA panel in plasma was identified as a potential biomarker for lung adenocarcinoma diagnosis. Oncotarget 2017; 8(4): 6513–6525
Pubmed
[75]
Miranda-Castro R, Palchetti I, de-Los-Santos-Álvarez N. The translational potential of electrochemical DNA-based liquid biopsy. Front Chem 2020; 8: 143
CrossRef Pubmed Google scholar
[76]
Díaz-Fernández A, Lorenzo-Gómez R, Miranda-Castro R, de-Los-Santos-Álvarez N, Lobo-Castañón MJ. Electrochemical aptasensors for cancer diagnosis in biological fluids—a review. Anal Chim Acta 2020; 1124: 1–19
CrossRef Pubmed Google scholar
[77]
Abi A, Mohammadpour Z, Zuo X, Safavi A. Nucleic acid-based electrochemical nanobiosensors. Biosens Bioelectron 2018; 102: 479–489
CrossRef Pubmed Google scholar
[78]
Yin X, Hou T, Huang B, Yang L, Li F. Aptamer recognition-trigged label-free homogeneous electrochemical strategy for an ultrasensitive cancer-derived exosome assay. Chem Commun (Camb) 2019; 55(91): 13705–13708
CrossRef Pubmed Google scholar
[79]
Dong H, Chen H, Jiang J, Zhang H, Cai C, Shen Q. Highly sensitive electrochemical detection of tumor exosomes based on aptamer recognition-induced multi-DNA release and cyclic enzymatic amplification. Anal Chem 2018; 90(7): 4507–4513
CrossRef Pubmed Google scholar
[80]
Zhao L, Sun R, He P, Zhang X. Ultrasensitive detection of exosomes by target-triggered three-dimensional DNA walking machine and exonuclease III-assisted electrochemical ratiometric biosensing. Anal Chem 2019; 91(22): 14773–14779
CrossRef Pubmed Google scholar
[81]
Wang L, Zeng L, Wang Y, Chen T, Chen W, Chen G, Li C, Chen J. Electrochemical aptasensor based on multidirectional hybridization chain reaction for detection of tumorous exosomes. Sens Actuators B Chem 2021; 332: 129471
CrossRef Google scholar
[82]
An Y, Jin T, Zhu Y, Zhang F, He P. An ultrasensitive electrochemical aptasensor for the determination of tumor exosomes based on click chemistry. Biosens Bioelectron 2019; 142: 111503
CrossRef Pubmed Google scholar
[83]
Cao Y, Li L, Han B, Wang Y, Dai Y, Zhao J. A catalytic molecule machine-driven biosensing method for amplified electrochemical detection of exosomes. Biosens Bioelectron 2019; 141: 111397
CrossRef Pubmed Google scholar
[84]
McLean MH, El-Omar EM. Genetics of gastric cancer. Nat Rev Gastroenterol Hepatol 2014; 11(11): 664–674
CrossRef Pubmed Google scholar
[85]
Huang R, He L, Xia Y, Xu H, Liu C, Xie H, Wang S, Peng L, Liu Y, Liu Y, He N, Li Z. A sensitive aptasensor based on a hemin/G-quadruplex-assisted signal amplification strategy for electrochemical detection of gastric cancer exosomes. Small 2019; 15(19): e1900735
CrossRef Pubmed Google scholar
[86]
Wang L, Deng Y, Wei J, Huang Y, Wang Z, Li G. Spherical nucleic acids-based cascade signal amplification for highly sensitive detection of exosomes. Biosens Bioelectron 2021; 191: 113465
CrossRef Pubmed Google scholar
[87]
Maduraiveeran G, Sasidharan M, Ganesan V. Electrochemical sensor and biosensor platforms based on advanced nanomaterials for biological and biomedical applications. Biosens Bioelectron 2018; 103: 113–129
CrossRef Pubmed Google scholar
[88]
Kreno LE, Leong K, Farha OK, Allendorf M, Van Duyne RP, Hupp JT. Metal-organic framework materials as chemical sensors. Chem Rev 2012; 112(2): 1105–1125
CrossRef Pubmed Google scholar
[89]
Heck JG, Napp J, Simonato S, Möllmer J, Lange M, Reichardt HM, Staudt R, Alves F, Feldmann C. Multifunctional phosphate-based inorganic-organic hybrid nanoparticles. J Am Chem Soc 2015; 137(23): 7329–7336
CrossRef Pubmed Google scholar
[90]
Mao J, Ran D, Xie C, Shen Q, Wang S, Lu W. EGFR/EGFRvIII dual-targeting peptide-mediated drug delivery for enhanced glioma therapy. ACS Appl Mater Interfaces 2017; 9(29): 24462–24475
CrossRef Pubmed Google scholar
[91]
Cheng G, Li W, Ha L, Han X, Hao S, Wan Y, Wang Z, Dong F, Zou X, Mao Y, Zheng SY. Self-assembly of extracellular vesicle-like metal-organic framework nanoparticles for protection and intracellular delivery of biofunctional proteins. J Am Chem Soc 2018; 140(23): 7282–7291
CrossRef Pubmed Google scholar
[92]
Cao Y, Wang Y, Yu X, Jiang X, Li G, Zhao J. Identification of programmed death ligand-1 positive exosomes in breast cancer based on DNA amplification-responsive metal-organic frameworks. Biosens Bioelectron 2020; 166: 112452
CrossRef Pubmed Google scholar
[93]
Kandambeth S, Dey K, Banerjee R. Covalent organic frameworks: chemistry beyond the structure. J Am Chem Soc 2019; 141(5): 1807–1822
CrossRef Pubmed Google scholar
[94]
Wang M, Pan Y, Wu S, Sun Z, Wang L, Yang J, Yin Y, Li G. Detection of colorectal cancer-derived exosomes based on covalent organic frameworks. Biosens Bioelectron 2020; 169: 112638
CrossRef Pubmed Google scholar
[95]
Farhana FZ, Umer M, Saeed A, Pannu AS, Shahbazi M, Jabur A, Nam HJ, Ostrikov K, Sonar P, Firoz SH, Shiddiky MJA. Isolation and detection of exosomes using Fe2O3 nanoparticles. ACS Appl Nano Mater 2021; 4(2): 1175–1186
CrossRef Google scholar
[96]
Xu L, Shoaie N, Jahanpeyma F, Zhao J, Azimzadeh M, Al Jamal KT. Optical, electrochemical and electrical (nano)biosensors for detection of exosomes: a comprehensive overview. Biosens Bioelectron 2020; 161: 112222
CrossRef Pubmed Google scholar
[97]
Kholafazad Kordasht H, Hasanzadeh M. Biomedical analysis of exosomes using biosensing methods: recent progress. Anal Methods 2020; 12(22): 2795–2811
CrossRef Pubmed Google scholar
[98]
Panagopoulou MS, Wark AW, Birch DJS, Gregory CD. Phenotypic analysis of extracellular vesicles: a review on the applications of fluorescence. J Extracell Vesicles 2020; 9(1): 1710020
CrossRef Pubmed Google scholar
[99]
Wang L, Yang Y, Liu Y, Ning L, Xiang Y, Li G. Bridging exosome and liposome through zirconium-phosphate coordination chemistry: a new method for exosome detection. Chem Commun (Camb) 2019; 55(18): 2708–2711
CrossRef Pubmed Google scholar
[100]
Yu X, He L, Pentok M, Yang H, Yang Y, Li Z, He N, Deng Y, Li S, Liu T, Chen X, Luo H. An aptamer-based new method for competitive fluorescence detection of exosomes. Nanoscale 2019; 11(33): 15589–15595
CrossRef Pubmed Google scholar
[101]
Pan Y, Wang L, Deng Y, Wang M, Peng Y, Yang J, Li G. A simple and sensitive method for exosome detection based on steric hindrance-controlled signal amplification. Chem Commun (Camb) 2020; 56(89): 13768–13771
CrossRef Pubmed Google scholar
[102]
Tian W, Li P, He W, Liu C, Li Z. Rolling circle extension-actuated loop-mediated isothermal amplification (RCA-LAMP) for ultrasensitive detection of microRNAs. Biosens Bioelectron 2019; 128: 17–22
CrossRef Pubmed Google scholar
[103]
Huang L, Wang DB, Singh N, Yang F, Gu N, Zhang XE. A dual-signal amplification platform for sensitive fluorescence biosensing of leukemia-derived exosomes. Nanoscale 2018; 10(43): 20289–20295
CrossRef Pubmed Google scholar
[104]
Huang R, He L, Li S, Liu H, Jin L, Chen Z, Zhao Y, Li Z, Deng Y, He N. A simple fluorescence aptasensor for gastric cancer exosome detection based on branched rolling circle amplification. Nanoscale 2020; 12(4): 2445–2451
CrossRef Pubmed Google scholar
[105]
Zhang J, Shi J, Liu W, Zhang K, Zhao H, Zhang H, Zhang Z. A simple, specific and “on-off” type MUC1 fluorescence aptasensor based on exosomes for detection of breast cancer. Sens Actuators B Chem 2018; 276: 552–559
CrossRef Google scholar
[106]
Li P, Yu X, Han W, Kong Y, Bao W, Zhang J, Zhang W, Gu Y. Ultrasensitive and reversible nanoplatform of urinary exosomes for prostate cancer diagnosis. ACS Sens 2019; 4(5): 1433–1441
CrossRef Pubmed Google scholar
[107]
Yu Y, Zhang WS, Guo Y, Peng H, Zhu M, Miao D, Su G. Engineering of exosome-triggered enzyme-powered DNA motors for highly sensitive fluorescence detection of tumor-derived exosomes. Biosens Bioelectron 2020; 167: 112482
CrossRef Pubmed Google scholar
[108]
Li B, Liu C, Pan W, Shen J, Guo J, Luo T, Feng J, Situ B, An T, Zhang Y, Zheng L. Facile fluorescent aptasensor using aggregation-induced emission luminogens for exosomal proteins profiling towards liquid biopsy. Biosens Bioelectron 2020; 168: 112520
CrossRef Pubmed Google scholar
[109]
Zhang Z, Tang C, Zhao L, Xu L, Zhou W, Dong Z, Yang Y, Xie Q, Fang X. Aptamer-based fluorescence polarization assay for separation-free exosome quantification. Nanoscale 2019; 11(20): 10106–10113
CrossRef Pubmed Google scholar
[110]
Liang X, Han L. White peroxidase-mimicking nanozymes: colorimetric pesticide assay without interferences of O2 and color. Adv Funct Mater 2020; 30(28): 2001933
CrossRef Google scholar
[111]
Xu L, Chopdat R, Li D, Al-Jamal KT. Development of a simple, sensitive and selective colorimetric aptasensor for the detection of cancer-derived exosomes. Biosens Bioelectron 2020; 169: 112576
CrossRef Pubmed Google scholar
[112]
Mokhtarzadeh A, Ezzati Nazhad Dolatabadi J, Abnous K, de la Guardia M, Ramezani M. Nanomaterial-based cocaine aptasensors. Biosens Bioelectron 2015; 68: 95–106
CrossRef Pubmed Google scholar
[113]
Liu W, Li J, Wu Y, Xing S, Lai Y, Zhang G. Target-induced proximity ligation triggers recombinase polymerase amplification and transcription-mediated amplification to detect tumor-derived exosomes in nasopharyngeal carcinoma with high sensitivity. Biosens Bioelectron 2018; 102: 204–210PMID:29145073
CrossRef Google scholar
[114]
Li J, Baird MA, Davis MA, Tai W, Zweifel LS, Adams Waldorf KM, Gale M Jr, Rajagopal L, Pierce RH, Gao X. Dramatic enhancement of the detection limits of bioassays via ultrafast deposition of polydopamine. Nat Biomed Eng 2017; 1: 0082
CrossRef Pubmed Google scholar
[115]
Lee H, Rho J, Messersmith PB. Facile conjugation of biomolecules onto surfaces via mussel adhesive protein inspired coatings. Adv Mater 2009; 21(4): 431–434
CrossRef Pubmed Google scholar
[116]
Chen Z, Cheng SB, Cao P, Qiu QF, Chen Y, Xie M, Xu Y, Huang WH. Detection of exosomes by ZnO nanowires coated three-dimensional scaffold chip device. Biosens Bioelectron 2018; 122: 211–216
CrossRef Pubmed Google scholar
[117]
He F, Liu H, Guo X, Yin BC, Ye BC. Direct exosome quantification via bivalent-cholesterol-labeled DNA anchor for signal amplification. Anal Chem 2017; 89(23): 12968–12975
CrossRef Pubmed Google scholar
[118]
Zhang Y, Wang D, Yue S, Lu Y, Yang C, Fang J, Xu Z. Sensitive multicolor visual detection of exosomes via dual signal amplification strategy of enzyme-catalyzed metallization of Au nanorods and hybridization chain reaction. ACS Sens 2019; 4(12): 3210–3218
CrossRef Pubmed Google scholar
[119]
Zhang Y, Jiao J, Wei Y, Wang D, Yang C, Xu Z. Plasmonic colorimetric biosensor for sensitive exosome detection via enzyme-induced etching of gold nanobipyramid@MnO2 nanosheet nanostructures. Anal Chem 2020; 92(22): 15244–15252
CrossRef Pubmed Google scholar
[120]
Munir S, Shah AA, Rahman H, Bilal M, Rajoka MSR, Khan AA, Khurshid M. Nanozymes for medical biotechnology and its potential applications in biosensing and nanotherapeutics. Biotechnol Lett 2020; 42(3): 357–373
CrossRef Pubmed Google scholar
[121]
Chen J, Xu Y, Lu Y, Xing W. Isolation and visible detection of tumor-derived exosomes from plasma. Anal Chem 2018; 90(24): 14207–14215
CrossRef Pubmed Google scholar
[122]
Boriachek K, Masud MK, Palma C, Phan HP, Yamauchi Y, Hossain MSA, Nguyen NT, Salomon C, Shiddiky MJA. Avoiding pre-isolation step in exosome analysis: direct isolation and sensitive detection of exosomes using gold-loaded nanoporous ferric oxide nanozymes. Anal Chem 2019; 91(6): 3827–3834
CrossRef Pubmed Google scholar
[123]
Wang YM, Liu JW, Adkins GB, Shen W, Trinh MP, Duan LY, Jiang JH, Zhong W. Enhancement of the intrinsic peroxidase-like activity of graphitic carbon nitride nanosheets by ssDNAs and its application for detection of exosomes. Anal Chem 2017; 89(22): 12327–12333
CrossRef Pubmed Google scholar
[124]
Xia Y, Liu M, Wang L, Yan A, He W, Chen M, Lan J, Xu J, Guan L, Chen J. A visible and colorimetric aptasensor based on DNA-capped single-walled carbon nanotubes for detection of exosomes. Biosens Bioelectron 2017; 92: 8–15
CrossRef Pubmed Google scholar
[125]
Zhou Y, Xu H, Wang H, Ye BC. Detection of breast cancer-derived exosomes using the horseradish peroxidase-mimicking DNAzyme as an aptasensor. Analyst (Lond) 2020; 145: 107–114
CrossRef Pubmed Google scholar
[126]
Masson JF. Surface plasmon resonance clinical biosensors for medical diagnostics. ACS Sens 2017; 2(1): 16–30
CrossRef Pubmed Google scholar
[127]
Singh P, Biosensors SPR. Historical perspectives and current challenges. Sens Actuators B Chem 2016; 229: 110–130
CrossRef Google scholar
[128]
Kabashin AV, Evans P, Pastkovsky S, Hendren W, Wurtz GA, Atkinson R, Pollard R, Podolskiy VA, Zayats AV. Plasmonic nanorod metamaterials for biosensing. Nat Mater 2009; 8(11): 867–871
CrossRef Pubmed Google scholar
[129]
Wang Q, Zou L, Yang X, Liu X, Nie W, Zheng Y, Cheng Q, Wang K. Direct quantification of cancerous exosomes via surface plasmon resonance with dual gold nanoparticle-assisted signal amplification. Biosens Bioelectron 2019; 135: 129–136
CrossRef Pubmed Google scholar
[130]
Thakur A, Qiu G, Ng SP, Guan J, Yue J, Lee Y, Wu CL. Direct detection of two different tumor-derived extracellular vesicles by SAM-AuNIs LSPR biosensor. Biosens Bioelectron 2017; 94: 400–407
CrossRef Pubmed Google scholar
[131]
Qiu G, Thakur A, Xu C, Ng SP, Lee Y, Wu CML. Detection of glioma-derived exosomes with the biotinylated antibody-functionalized titanium nitride plasmonic biosensor. Adv Funct Mater 2019; 29(9): 1806761
CrossRef Google scholar
[132]
Im H, Shao H, Park YI, Peterson VM, Castro CM, Weissleder R, Lee H. Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor. Nat Biotechnol 2014; 32(5): 490–495
CrossRef Pubmed Google scholar
[133]
Zong S, Wang Z, Chen H, Cui Y. Ultrasensitive telomerase activity detection by telomeric elongation controlled surface enhanced Raman scattering. Small 2013; 9(24): 4215–4220
CrossRef Pubmed Google scholar
[134]
Cialla-May D, Zheng XS, Weber K, Popp J. Recent progress in surface-enhanced Raman spectroscopy for biological and biomedical applications: from cells to clinics. Chem Soc Rev 2017; 46(13): 3945–3961
CrossRef Pubmed Google scholar
[135]
Wang Z, Zong S, Wang Y, Li N, Li L, Lu J, Wang Z, Chen B, Cui Y. Screening and multiple detection of cancer exosomes using an SERS-based method. Nanoscale 2018; 10(19): 9053–9062
CrossRef Pubmed Google scholar
[136]
Zong S, Wang L, Chen C, Lu J, Zhu D, Zhang Y, Wang Z, Cui Y. Facile detection of tumor-derived exosomes using magnetic nanobeads and SERS nanoprobes. Anal Methods 2016; 8(25): 5001–5008
CrossRef Google scholar
[137]
Kwizera EA, O’Connor R, Vinduska V, Williams M, Butch ER, Snyder SE, Chen X, Huang X. Molecular detection and analysis of exosomes using surface-enhanced Raman scattering gold nanorods and a miniaturized device. Theranostics 2018; 8(10): 2722–2738
CrossRef Pubmed Google scholar
[138]
Ma D, Huang C, Zheng J, Tang J, Li J, Yang J, Yang R. Quantitative detection of exosomal microRNA extracted from human blood based on surface-enhanced Raman scattering. Biosens Bioelectron 2018; 101: 167–173
CrossRef Pubmed Google scholar
[139]
Lee JU, Kim WH, Lee HS, Park KH, Sim SJ. Quantitative and specific detection of exosomal miRNAs for accurate diagnosis of breast cancer using a surface-enhanced Raman scattering sensor based on plasmonic head-flocked gold nanopillars. Small 2019; 15(17): e1804968
CrossRef Pubmed Google scholar
[140]
Sackmann EK, Fulton AL, Beebe DJ. The present and future role of microfluidics in biomedical research. Nature 2014; 507(7491): 181–189
CrossRef Pubmed Google scholar
[141]
Chen W, Shao F, Xianyu Y. Microfluidics-implemented biochemical assays: from the perspective of readout. Small 2020; 16(9): e1903388
CrossRef Pubmed Google scholar
[142]
Kanwar SS, Dunlay CJ, Simeone DM, Nagrath S. Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip 2014; 14(11): 1891–1900
CrossRef Pubmed Google scholar
[143]
Zhang P, He M, Zeng Y. Ultrasensitive microfluidic analysis of circulating exosomes using a nanostructured graphene oxide/polydopamine coating. Lab Chip 2016; 16(16): 3033–3042
CrossRef Pubmed Google scholar
[144]
Vaidyanathan R, Naghibosadat M, Rauf S, Korbie D, Carrascosa LG, Shiddiky MJA, Trau M. Detecting exosomes specifically: a multiplexed device based on alternating current electrohydrodynamic induced nanoshearing. Anal Chem 2014; 86(22): 11125–11132
CrossRef Pubmed Google scholar
[145]
Woo HK, Sunkara V, Park J, Kim TH, Han JR, Kim CJ, Choi HI, Kim YK, Cho YK. Exodisc for rapid, size-selective, and efficient isolation and analysis of nanoscale extracellular vesicles from biological samples. ACS Nano 2017; 11(2): 1360–1370
CrossRef Pubmed Google scholar
[146]
Liang LG, Kong MQ, Zhou S, Sheng YF, Wang P, Yu T, Inci F, Kuo WP, Li LJ, Demirci U, Wang S. An integrated double-filtration microfluidic device for isolation, enrichment and quantification of urinary extracellular vesicles for detection of bladder cancer. Sci Rep 2017; 7(1): 46224
CrossRef Pubmed Google scholar
[147]
Zhu L, Wang K, Cui J, Liu H, Bu X, Ma H, Wang W, Gong H, Lausted C, Hood L, Yang G, Hu Z. Label-free quantitative detection of tumor-derived exosomes through surface plasmon resonance imaging. Anal Chem 2014; 86(17): 8857–8864
CrossRef Pubmed Google scholar
[148]
Shao H, Chung J, Balaj L, Charest A, Bigner DD, Carter BS, Hochberg FH, Breakefield XO, Weissleder R, Lee H. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med 2012; 18(12): 1835–1840
CrossRef Pubmed Google scholar
[149]
Shin SR, Kilic T, Zhang YS, Avci H, Hu N, Kim D, Branco C, Aleman J, Massa S, Silvestri A, Kang J, Desalvo A, Hussaini MA, Chae SK, Polini A, Bhise N, Hussain MA, Lee H, Dokmeci MR, Khademhosseini A. Label-free and regenerative electrochemical microfluidic biosensors for continual monitoring of cell secretomes. Adv Sci (Weinh) 2017; 4(5): 1600522
CrossRef Pubmed Google scholar
[150]
Hamada T, Keum N, Nishihara R, Ogino S. Molecular pathological epidemiology: new developing frontiers of big data science to study etiologies and pathogenesis. J Gastroenterol 2017; 52(3): 265–275
CrossRef Pubmed Google scholar

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 81772593).

Compliance with ethics guidelines

Ying Deng, Zhaowei Sun, Lei Wang, Minghui Wang, Jie Yang, and Genxi Li declare that they have no conflict of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

Open Access

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
To view a copy of this license, visit https://creativecommons.org/licenses/by/4.0/.

RIGHTS & PERMISSIONS

2021 The Author(s) 2021. This article is published with open access at link.springer.com and journal.hep.com.cn
AI Summary AI Mindmap
PDF(2667 KB)

Accesses

Citations

Detail

Sections
Recommended

/