Abstract
Noninvasive examination is an emerging area in the field of neuro-oncology. Liquid biopsy captures the landscape of genomic alterations of brain tumors and revolutionizes the traditional diagnosis approaches. Rapidly changing sequencing technologies and more affordable prices put the screws on more application of liquid biopsy in clinical settings. In the past few years, extensive application of liquid biopsy has been seen throughout the whole diagnosis and treatment process of brain tumors, including early and accurate detection, characterization and dynamic monitoring. Here, we summarized and compared the most advanced techniques and target molecules or macrostructures related to brain tumor liquid biopsy. We further reviewed and emphasized recent progression in different clinical settings for brain tumors in blood and CSF. The preferred protocol, potential novel biomarkers and future development are discussed in the last part.
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Data availability
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- AUC:
-
Area under curve
- BBB:
-
Blood–brain barrier
- BEAMing:
-
Beads, emulsion, amplification, and magnetics
- BM:
-
Brain metastases
- cfDNA:
-
Circulating free DNA
- CNS:
-
Central nervous system
- CNV:
-
Copy number variations
- CSF:
-
Cerebrospinal fluid
- CTC:
-
Circulating tumor cells
- ctDNA:
-
Circulating tumor DNA
- ddPCR:
-
Droplet digital polymerase chain reaction
- DMG:
-
Diffuse midline glioma
- DSC:
-
Differential scanning calorimetry
- EGFR:
-
Epidermal growth factor receptor
- EV:
-
Extracellular vesicle
- FTIR spectroscopy:
-
Fourier transform infrared spectroscopy
- GBM:
-
Glioblastomas
- GSC:
-
Glioblastoma stem cell
- HGG:
-
High-grade glioma
- IDH:
-
Isocitrate dehydrogenase
- LC–MS:
-
Liquid chromatography-mass spectrometry
- LGG:
-
Low-grade glioma
- LM:
-
Leptomeningeal metastases
- MB:
-
Medulloblastoma
- MGMT:
-
O6-methylguanine-DNA methyltransferase
- MV:
-
Microvesicle
- nanoDSF:
-
Nano differential scanning fluorimetry
- NGS:
-
Next-generation sequencing
- NSCLC:
-
Non-smal cell lung cancer
- PAP:
-
Pyrophosphorolysis-activated polymerization
- SCNA:
-
Somatic copy number alteration
- SVM:
-
Supporting vector machine
- TAM-seq:
-
Tagged-amplicon deep sequencing
- TCA:
-
Tricarboxylic acid cycle
- TEP:
-
Tumor-educated platelet
- TERT:
-
Telomerase reverse transcriptase
- WES:
-
Whole-exosome sequencing
- WGS:
-
Whole-genome sequencing
References
Aceto N et al (2015) En route to metastasis: circulating tumor cell clusters and epithelial-to-mesenchymal transition. Trends Cancer 1(1):44–52
Acinas SG et al (2005) PCR-induced sequence artifacts and bias: insights from comparison of two 16S rRNA clone libraries constructed from the same sample. Appl Environ Microbiol 71(12):8966–8969
Aldea M et al (2020) Circulating tumor DNA analysis for patients with oncogene-addicted NSCLC with isolated central nervous system progression. J Thoracic Oncol 15(3):383–391
Ali N et al (2017) Current nucleic acid extraction methods and their implications to point-of-care diagnostics. Biomed Res Int 2017:9306564
Alix-Panabières C, Pantel K (2013) Circulating tumor cells: liquid biopsy of cancer. Clin Chem 59(1):110–118
Ballester LY et al (2018) Analysis of cerebrospinal fluid metabolites in patients with primary or metastatic central nervous system tumors. Acta Neuropathol Commun 6(1):85
Baraniskin A et al (2011) Identification of microRNAs in the cerebrospinal fluid as marker for primary diffuse large B-cell lymphoma of the central nervous system. Blood 117(11):3140–3146
Baraniskin A et al (2012) Identification of microRNAs in the cerebrospinal fluid as biomarker for the diagnosis of glioma. Neuro Oncol 14(1):29–33
Barthel FP, Wesseling P, Verhaak RGW (2018) Reconstructing the molecular life history of gliomas. Acta Neuropathol 135(5):649–670
Best MG et al (2015) RNA-seq of tumor-educated platelets enables blood-based pan-cancer, multiclass, and molecular pathway cancer diagnostics. Cancer Cell 28(5):666–676
Best MG et al (2017) Swarm intelligence-enhanced detection of non-small-cell lung cancer using tumor-educated platelets. Cancer Cell 32(2):238-252.e9
Best MG, Wesseling P, Wurdinger T (2018) Tumor-educated platelets as a noninvasive biomarker source for cancer detection and progression monitoring. Can Res 78(13):3407–3412
Best MG et al (2019) RNA sequencing and swarm intelligence-enhanced classification algorithm development for blood-based disease diagnostics using spliced blood platelet RNA. Nat Protoc 14(4):1206–1234
Bettegowda C et al (2014) Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 6(224):224ra24
Billard P et al (2021) The TeloDIAG: how telomeric parameters can help in glioma rapid diagnosis and liquid biopsy approaches. Ann Oncol 32(12):1608–1617
Bobillo S et al (2021) Cell free circulating tumor DNA in cerebrospinal fluid detects and monitors central nervous system involvement of B-cell lymphomas. Haematologica 106(2):513–521
Butler TM, Spellman PT, Gray J (2017) Circulating-tumor DNA as an early detection and diagnostic tool. Curr Opin Genet Dev 42:14–21
Calabrese C et al (2020) Genomic basis for RNA alterations in cancer. Nature 578:129–136
Campanella R et al (2020) Tumor-educated platelets and angiogenesis in glioblastoma: another brick in the wall for novel prognostic and targetable biomarkers, changing the vision from a localized tumor to a systemic pathology. Cells 9(2):294
Capper D et al (2010) Characterization of R132H mutation-specific IDH1 antibody binding in brain tumors. Brain Pathol (zurich, Switzerland) 20(1):245–254
Capper D et al (2011) Assessment of BRAF V600E mutation status by immunohistochemistry with a mutation-specific monoclonal antibody. Acta Neuropathol 122(1):11–19
Carlino MS et al (2015) Targeting oncogenic BRAF and aberrant MAPK activation in the treatment of cutaneous melanoma. Crit Rev Oncol Hematol 96(3):385–398
Chagovetz AA et al (2013) Differential scanning calorimetry of gliomas: a new tool in brain cancer diagnostics? Neurosurgery 73(2):289–295
Chan K et al (2005) Effects of preanalytical factors on the molecular size of cell-free DNA in blood. Clin Chem 51(4):781–784
Cohen JD et al (2018) Detection and localization of surgically resectable cancers with a multi-analyte blood test. Science 359(6378):926–930
Colombo M, Raposo G, Théry C (2014) Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 30:255–289
Cucchiara F et al (2020) Integrating liquid biopsy and radiomics to monitor clonal heterogeneity of EGFR-positive non-small cell lung cancer. Front Oncol 10:593831
Dawson S et al (2013) Analysis of circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med 368(13):1199–1209
Di Meo A et al (2017) Liquid biopsy: a step forward towards precision medicine in urologic malignancies. Mol Cancer 16(1):80
Di Vito C et al (2017) Platelets from glioblastoma patients promote angiogenesis of tumor endothelial cells and exhibit increased VEGF content and release. Platelets 28(6):585–594
Diaz LAJ, Bardelli A (2014) Liquid biopsies: genotyping circulating tumor DNA. J Clin Oncol 32(6):579–586
Diehl F et al (2008) Circulating mutant DNA to assess tumor dynamics. Nat Med 14(9):985–990
Diplas BH et al (2019) Sensitive and rapid detection of TERT promoter and IDH mutations in diffuse gliomas. Neuro Oncol 21(4):440–450
El Messaoudi S et al (2013) Circulating cell free DNA: preanalytical considerations. Clin Chim Acta 424:222–230
Engh JA (2011) Differential scanning calorimetry applied to cerebrospinal fluid analysis in glioblastoma. Neurosurgery 69(4):N22–N23
Erpenbeck L, Schön MP (2010) Deadly allies: the fatal interplay between platelets and metastasizing cancer cells. Blood 115(17):3427–3436
Escudero L et al (2020) Circulating tumour DNA from the cerebrospinal fluid allows the characterisation and monitoring of medulloblastoma. Nat Commun 11(1):5376
Fanfani V et al (2021) The landscape of the heritable cancer genome. Cancer Res 81(10):2588–2599
Fernando MR et al (2017) New evidence that a large proportion of human blood plasma cell-free DNA is localized in exosomes. PLoS ONE 12(8):e0183915
Figueroa JM et al (2017) Detection of wild-type EGFR amplification and EGFRvIII mutation in CSF-derived extracellular vesicles of glioblastoma patients. Neuro Oncol 19(11):1494–1502
Fleischhacker M, Schmidt B (2007) Circulating nucleic acids (CNAs) and cancer–a survey. Biochem Biophys Acta 1775(1):181–232
Fonkem E, Lun M, Wong ET (2011) Rare phenomenon of extracranial metastasis of glioblastoma. J Clin Oncol 29(34):4594–4595
García-Romero N et al (2019) BRAF V600E detection in liquid biopsies from pediatric central nervous system tumors. Cancers 12(1):66
Gautschi O et al (2004) Circulating deoxyribonucleic acid as prognostic marker in non-small-cell lung cancer patients undergoing chemotherapy. J Clin Oncol 22(20):4157–4164
Gay LJ, Felding-Habermann B (2011) Contribution of platelets to tumour metastasis. Nat Rev Cancer 11(2):123–134
Geraldo LHM et al (2019) Glioblastoma therapy in the age of molecular medicine. Trends Cancer 5(1):46–65
Godlewski J et al (2010) MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells. Mol Cell 37(5):620–632
Grommes C et al (2019) Phase 1b trial of an ibrutinib-based combination therapy in recurrent/refractory CNS lymphoma. Blood 133(5):436–445
Hansen TB et al (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495(7441):384–388
Haque IS, Elemento O (2017) Challenges in using ctDNA to achieve early detection of cancer. bioRxiv. https://doi.org/10.1101/237578
Hermoso-Durán S et al (2020) Thermal liquid biopsy (TLB) focused on benign and premalignant pancreatic cyst diagnosis. J Personalized Med 11(1):25
Huang TY et al (2017) Detection of Histone H3 mutations in cerebrospinal fluid-derived tumor DNA from children with diffuse midline glioma. Acta Neuropathol Commun 5(1):28
Ignatiadis M, Sledge GW, Jeffrey SS (2021) Liquid biopsy enters the clinic - implementation issues and future challenges. Nat Rev Clin Oncol 18(5):297–312
Indira Chandran V et al (2019) Ultrasensitive immunoprofiling of plasma extracellular vesicles identifies syndecan-1 as a potential tool for minimally invasive diagnosis of glioma. Clin Cancer Res 25(10):3115–3127
Jahr S et al (2001) DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res 61(4):1659–1665
Jalali M et al (2021) Plasmonic nanobowtiefluidic device for sensitive detection of glioma extracellular vesicles by Raman spectrometry. Lab Chip 21(5):855–866
Jiang P et al (2015) Lengthening and shortening of plasma DNA in hepatocellular carcinoma patients. Proc Natl Acad Sci USA 112(11):E1317–E1325
Jiang B et al (2017a) Detection of driver and resistance mutations in leptomeningeal metastases of NSCLC by next-generation sequencing of cerebrospinal fluid circulating tumor cells. Clin Cancer Res 23(18):5480–5488
Jiang X et al (2017b) Microfluidic isolation of platelet-covered circulating tumor cells. Lab Chip 17(20):3498–3503
Jung M et al (2003) Changes in concentration of DNA in serum and plasma during storage of blood samples. Clin Chem 49(1):1028–1029
Kahlert C, Kalluri R (2013) Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (berl) 91(4):431–437
Kalokhe G et al (2012) Metastatic glioblastoma: case presentations and a review of the literature. J Neuro Oncol 107(1):21–27
Kammesheidt A et al (2016) Mutation detection in cell free DNA from healthy donors. J Clinical Oncol 34(15):e23054
Kane JR (2019) The role of brain vasculature in glioblastoma. Mol Neurobiol 56(9):6645–6653
Kang KM et al (2021) Blood-based detection of BRAF V600E in gliomas and brain tumor metastasis. Cancers 13(6):1227
Khuong-Quang D et al (2012) K27M mutation in histone H3.3 defines clinically and biologically distinct subgroups of pediatric diffuse intrinsic pontine gliomas. Acta Neuropathol 124(3):439–447
Khwaja FW et al (2006) Attractin is elevated in the cerebrospinal fluid of patients with malignant astrocytoma and mediates glioma cell migration. Clin Cancer Res 12(21):6331–6336
Khwaja FW et al (2007) Proteomic identification of biomarkers in the cerebrospinal fluid (CSF) of astrocytoma patients. J Proteome Res 6(2):559–570
Kilgour E et al (2020) Liquid biopsy-based biomarkers of treatment response and resistance. Cancer Cell 37(4):485–495
Kitamura T, Qian B, Pollard JW (2015) Immune cell promotion of metastasis. Nat Rev Immunol 15(2):73–86
Kitano Y et al (2021) Urinary MicroRNA-based diagnostic model for central nervous system tumors using nanowire scaffolds. ACS Appl Mater Interfaces 13(15):17316–17329
Konstantopoulos K, Thomas SN (2009) Cancer cells in transit: the vascular interactions of tumor cells. Annu Rev Biomed Eng 11:177–202
Krol I et al (2018) Detection of circulating tumour cell clusters in human glioblastoma. Br J Cancer 119(4):487–491
Kros JM et al (2015) Circulating glioma biomarkers. Neuro Oncol 17(3):343–360
Kulasinghe A et al (2017) Enrichment of circulating head and neck tumour cells using spiral microfluidic technology. Sci Rep 7:42517
Labelle M, Begum S, Hynes RO (2014) Platelets guide the formation of early metastatic niches. Proc Natl Acad Sci USA 111(30):E3053–E3061
Lassaletta A et al (2017) Therapeutic and prognostic implications of BRAF V600E in pediatric low-grade gliomas. J Clin Oncol 35(25):2934
Lawrence MS et al (2014) Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 505(7484):495–501
Lawson C et al (2016) Microvesicles and exosomes: new players in metabolic and cardiovascular disease. J Endocrinol 228(2):R57-71
Lee Y, El Andaloussi S, Wood MJA (2012) Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21(R1):R125–R134
Lennon AM et al (2020) Feasibility of blood testing combined with PET-CT to screen for cancer and guide intervention. Science (new York, NY) 369(6499):eabb9601
Li CCY et al (2013) Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol 10(8):1333–1344
Li Y et al (2015) Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res 25(8):981–984
Li YS et al (2018) Unique genetic profiles from cerebrospinal fluid cell-free DNA in leptomeningeal metastases of EGFR-mutant non-small-cell lung cancer: a new medium of liquid biopsy. Ann Oncol 29(4):945–952
Li J et al (2020) Reliable tumor detection by whole-genome methylation sequencing of cell-free DNA in cerebrospinal fluid of pediatric medulloblastoma. Sci Adv 6(42):5427
Li P et al (2021) Circular RNA sequencing reveals serum exosome circular RNA panel for high-grade astrocytoma diagnosis. Clin Chem 68(2):343
Lianidou ES et al (2010) What’s new on circulating tumor cells? A meeting report. Brest Cancer Res 12(4):307
Lin B et al (2021) Microfluidic-based exosome analysis for liquid biopsy. Small Methods 5(3):e2001131
Liu APY et al (2021) Serial assessment of measurable residual disease in medulloblastoma liquid biopsies. Cancer Cell 39(11):1519-1530.e4
Louis DN et al (2016) The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 131(6):803–820
Lucero R et al (2020) Glioma-derived miRNA-containing extracellular vesicles induce angiogenesis by reprogramming brain endothelial cells. Cell Rep 30(7):2065-2074.e4
Lui Y et al (2002) Predominant hematopoietic origin of cell-free DNA in plasma and serum after sex-mismatched bone marrow transplantation. Clin Chem 48(3):421–427
Ma L et al (2021) Sensitive detection and conjoint analysis of promoter methylation by conjugated polymers for differential diagnosis and prognosis of glioma. ACS Appl Mater Interfaces 13(8):9291–9299
Maas SLN et al (2020) Orally administered 5-aminolevulinic acid for isolation and characterization of circulating tumor-derived extracellular vesicles in glioblastoma patients. Cancers 12(11):3297
Maire CL et al (2021) Genome-wide methylation profiling of glioblastoma cell-derived extracellular vesicle DNA allows tumor classification. Neuro Oncol 23(7):1087–1099
Martignano F (2019) Cell-Free DNA: an Overview of Sample Types and Isolation Procedures. Methods Mol Biol (clifton, N.J.) 1909:13–27
McDonald BR et al (2019) Personalized circulating tumor DNA analysis to detect residual disease after neoadjuvant therapy in breast cancer. Sci Transl Med 11(504):7392
Meng S et al (2017) CircRNA: functions and properties of a novel potential biomarker for cancer. Mol Cancer 16(1):94
Meng Y et al (2021) MR-guided focused ultrasound liquid biopsy enriches circulating biomarkers in patients with brain tumors. Neuro Oncol 23(10):1789–1797
Miller AM et al (2019) Tracking tumour evolution in glioma through liquid biopsies of cerebrospinal fluid. Nature 565(7741):654–658
Miller KD et al (2021) Brain and other central nervous system tumor statistics, 2021. CA 71(5):381–406
Mouliere F et al (2011) High fragmentation characterizes tumour-derived circulating DNA. PLoS ONE 6(9):e23418
Mouliere F et al (2018) Detection of cell-free DNA fragmentation and copy number alterations in cerebrospinal fluid from glioma patients. EMBO Mol Med 10(12):e9323
Mouliere F et al (2021) Fragmentation patterns and personalized sequencing of cell-free DNA in urine and plasma of glioma patients. EMBO Mol Med 13(8):e12881
Müller C et al (2014) Hematogenous dissemination of glioblastoma multiforme. Sci Transl Med 6(247):247ra101
Muralidharan K et al (2021) TERT Promoter mutation analysis for blood-based diagnosis and monitoring of gliomas. Clin Cancer Res 27(1):169–178
Nash GF et al (2002) Platelets and cancer. Lancet Oncol 3(7):425–430
Nassiri F et al (2020) Detection and discrimination of intracranial tumors using plasma cell-free DNA methylomes. Nat Med 26(7):1044–1047
Nieswandt B et al (1999) Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Can Res 59(6):1295–1300
Nilsson RJA et al (2011) Blood platelets contain tumor-derived RNA biomarkers. Blood 118(13):3680–3683
Nishizaki T et al (2001) Detection of craniospinal dissemination of intracranial germ cell tumours based on serum and cerebrospinal fluid levels of tumour markers. J Clin Neurosci 8(1):27–30
Northcott PA et al (2017) The whole-genome landscape of medulloblastoma subtypes. Nature 547(7663):311–317
Palumbo JS et al (2005) Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood 105(1):178–185
Pan C et al (2019) Molecular profiling of tumors of the brainstem by sequencing of CSF-derived circulating tumor DNA. Acta Neuropathol 137(2):297–306
Panditharatna E et al (2018) Clinically Relevant and minimally invasive tumor surveillance of pediatric diffuse midline gliomas using patient-derived liquid biopsy. Clin Cancer Res 24(23):5850–5859
Pantel K, Alix-Panabières C (2010) Circulating tumour cells in cancer patients: challenges and perspectives. Trends Mol Med 16(9):398–406
Pasquier B et al (1980) Extraneural metastases of astrocytomas and glioblastomas: clinicopathological study of two cases and review of literature. Cancer 45(1):112–125
Patil DP et al (2016) m(6)A RNA methylation promotes XIST-mediated transcriptional repression. Nature 537(7620):369–373
Pittella-Silva F et al (2020) Plasma or serum: which is preferable for mutation detection in liquid biopsy? Clin Chem 66(7):946–957
Placke T et al (2012) Platelet-derived MHC class I confers a pseudonormal phenotype to cancer cells that subverts the antitumor reactivity of natural killer immune cells. Cancer Res 72(2):440–448
Qaddoumi I et al (2012) Diagnostic utility and correlation of tumor markers in the serum and cerebrospinal fluid of children with intracranial germ cell tumors. Child’s Nervous Syst 28(7):1017–1024
Raz T et al (2011) Protocol dependence of sequencing-based gene expression measurements. PLoS ONE 6(5):e19287
Ricklefs FL et al (2018) Immune evasion mediated by PD-L1 on glioblastoma-derived extracellular vesicles. Sci Adv 4(3):2766
Rodrigo A et al (2019) Thermal liquid biopsy (TLB): a predictive score derived from serum thermograms as a clinical tool for screening lung cancer patients. Cancers 11(7):1012
Romero A et al (2021) Comprehensive cross-platform comparison of methods for non-invasive EGFR mutation testing: results of the RING observational trial. Mol Oncol 15(1):43–56
Sabedot T et al (2021) A serum-based DNA methylation assay provides accurate detection of glioma. Neuro Oncol 23(9):1494–1508
Sabrkhany S, Griffioen AW, Egbrink MGOA (2011) The role of blood platelets in tumor angiogenesis. Biochem Biophys Acta 1815(2):189–196
Sala A et al (2020) Biofluid diagnostics by FTIR spectroscopy: a platform technology for cancer detection. Cancer Lett 477:122–130
Sanchez JN, Wang T, Cohen MS (2018) BRAF and MEK inhibitors: use and resistance in BRAF-mutated cancers. Drugs 78(5):549–566
Santangelo A et al (2018) A microRNA signature from serum exosomes of patients with glioma as complementary diagnostic biomarker. J Neurooncol 136(1):51–62
Scher HI et al (2009) Circulating tumour cells as prognostic markers in progressive, castration-resistant prostate cancer: a reanalysis of IMMC38 trial data. Lancet Oncol 10(3):233–239
Seoane J et al (2019) Cerebrospinal fluid cell-free tumour DNA as a liquid biopsy for primary brain tumours and central nervous system metastases. Ann Oncol 30(2):211–218
Serrano MJ et al (2020) Precision prevention and cancer interception: the new challenges of liquid biopsy. Cancer Discov 10(11):1635–1644
Shankar GM et al (2017) Liquid biopsy for brain tumors. Expert Rev Mol Diagn 17(10):943–947
Shah N, Lankerovich M, Lee H, Yoon JG, Schroeder B, Foltz G (2013) Exploration of the gene fusion landscape of glioblastoma using transcriptome sequencing and copy number data. BMC genomics 14(1):818. https://doi.org/10.1186/1471-2164-14-818
Shen F et al (2014) Proteomic analysis of cerebrospinal fluid: toward the identification of biomarkers for gliomas. Neurosurg Rev 37(3):367–380
Siegel RL et al (2021) Cancer Statistics, 2021. CA 71(1):7–33
Sim H et al (2019) Tissue 2-hydroxyglutarate as a biomarker for isocitrate dehydrogenase mutations in gliomas. Clin Cancer Res 25(11):3366–3373
Sol N, Wurdinger T (2017) Platelet RNA signatures for the detection of cancer. Cancer Metastasis Rev 36(2):263–272
Sol N et al (2020) Tumor-educated platelet RNA for the detection and (pseudo)progression monitoring of glioblastoma. Cell Rep Med 1(7):100101
Sprouse ML et al (2019) PMN-MDSCs enhance CTC metastatic properties through reciprocal interactions via ROS/Notch/Nodal signaling. Int J Mol Sci 20(8):1916
Srinivasan VM et al (2016) Modern management of medulloblastoma: molecular classification, outcomes, and the role of surgery. Surg Neurol Int 7(Suppl 44):S1135–S1141
Srivastava S et al (2019) Cancer overdiagnosis: a biological challenge and clinical dilemma. Nat Rev Cancer 19(6):349–358
Sullivan JP et al (2014) Brain tumor cells in circulation are enriched for mesenchymal gene expression. Cancer Discov 4(11):1299–1309
Teplyuk NM et al (2012) MicroRNAs in cerebrospinal fluid identify glioblastoma and metastatic brain cancers and reflect disease activity. Neuro Oncol 14(6):689–700
Thakur BK et al (2014) Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res 244(6):766–769
Thakur A et al (2017) Direct detection of two different tumor-derived extracellular vesicles by SAM-AuNIs LSPR biosensor. Biosens Bioelectron 94:400–407
Thakur A et al (2021) In vivo liquid biopsy for glioblastoma malignancy by the AFM and LSPR based sensing of exosomal CD44 and CD133 in a mouse model. Biosens Bioelectron 191:113476
Théry C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev 2(8):569–579
Thierry A et al (2010) Origin and quantification of circulating DNA in mice with human colorectal cancer xenografts. Nucleic Acids Res 38(18):6159–6175
Tsvetkov PO et al (2018) Differential scanning calorimetry of plasma in glioblastoma: toward a new prognostic / monitoring tool. Oncotarget 9(10):9391–9399
Tsvetkov PO et al (2021) An AI-powered blood test to detect cancer using NanoDSF. Cancers 13(6):1294
Umetani N, Hiramatsu S, Hoon DSB (2006) Higher amount of free circulating DNA in serum than in plasma is not mainly caused by contaminated extraneous DNA during separation. Ann N Y Acad Sci 1075:299–307
Underhill HR et al (2016) Fragment length of circulating tumor DNA. PLoS Genet 12(7):e1006162
van Bodegraven EJ et al (2019) Importance of GFAP isoform-specific analyses in astrocytoma. Glia 67(8):1417–1433
Velazquez-Campoy A et al (2018) Thermal liquid biopsy for monitoring melanoma patients under surveillance during treatment: a pilot study. Biochim Biophys Acta 1862(8):1701–1710
Wang Y et al (2015a) Detection of tumor-derived DNA in cerebrospinal fluid of patients with primary tumors of the brain and spinal cord. Proc Natl Acad Sci USA 112(31):9704–9709
Wang E et al (2015b) Predictive genomics: a cancer hallmark network framework for predicting tumor clinical phenotypes using genome sequencing data. Semin Cancer Biol 30:4–12
Wang H et al (2019) Evaluation of serum extracellular vesicles as noninvasive diagnostic markers of glioma. Theranostics 9(18):5347–5358
Wang F et al (2020) Cerebrospinal fluid-based metabolomics to characterize different types of brain tumors. J Neurol 267(4):984–993
Wang L, Yekula A, Muralidharan K, Small JL, Rosh ZS, Kang KM, Carter BS, Balaj L (2020) Novel Gene Fusions in Glioblastoma Tumor Tissue and Matched Patient Plasma. Cancers 12(5):1219. https://doi.org/10.3390/cancers12051219
Watanabe A et al (2006) Expression of syndecans, a heparan sulfate proteoglycan, in malignant gliomas: participation of nuclear factor-kappaB in upregulation of syndecan-1 expression. J Neurooncol 77(1):25–32
Watanabe S et al (2012) A highly sensitive and specific chemiluminescent enzyme immunoassay for placental alkaline phosphatase in the cerebrospinal fluid of patients with intracranial germinomas. Pediatr Neurosurg 48(3):141–145
Weber C, Springer TA (1997) Neutrophil accumulation on activated, surface-adherent platelets in flow is mediated by interaction of Mac-1 with fibrinogen bound to alphaIIbbeta3 and stimulated by platelet-activating factor. J Clin Investig 100(8):2085–2093
Wei B et al (2019) Combined plasma and tissue genotyping of EGFR T790M benefits NSCLC patients: a real-world clinical example. Mol Oncol 13(5):1226–1234
Wong F et al (2016) Cell-free DNA in maternal plasma and serum: a comparison of quantity, quality and tissue origin using genomic and epigenomic approaches. Clin Biochem 49(18):1379–1386
Wu X et al (2020) Circulating tumor DNA as an emerging liquid biopsy biomarker for early diagnosis and therapeutic monitoring in hepatocellular carcinoma. Int J Biol Sci 16(9):1551–1562
Xu H et al (2018) NFIX circular RNA promotes glioma progression by regulating miR-34a-5p via notch signaling pathway. Front Mol Neurosci 11:225
Yin K, Liu X (2020) CircMMP1 promotes the progression of glioma through miR-433/HMGB3 axis in vitro and in vivo. IUBMB Life 72(11):2508–2524
Zeng A et al (2018) Exosomal transfer of miR-151a enhances chemosensitivity to temozolomide in drug-resistant glioblastoma. Cancer Lett 436:10–21
Zhang M et al (2018) A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma. Nat Commun 9(1):4475
Zhang B et al (2020) m(6)A regulator-mediated methylation modification patterns and tumor microenvironment infiltration characterization in gastric cancer. Mol Cancer 19(1):53
Zhang B et al (2021) m(6)A target microRNAs in serum for cancer detection. Mol Cancer 20(1):170
Zhao Y et al (2020) Cytoplasm protein GFAP magnetic beads construction and application as cell separation target for brain tumors. J Nanobiotechnol 18(1):169
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We are grateful to all of those with whom we have had the pleasure to work during this and other related projects.
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The research was funded by China Postdoctoral Science Foundation 2018M643006.
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ZY and YZ reviewed the literature and wrote the manuscript. CQ reviewed the literature and generated Table 2. YZ and ZL designed the research. All authors contributed to writing and critically revising the manuscript.
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Yi, Z., Qu, C., Zeng, Y. et al. Liquid biopsy: early and accurate diagnosis of brain tumor. J Cancer Res Clin Oncol 148, 2347–2373 (2022). https://doi.org/10.1007/s00432-022-04011-3
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DOI: https://doi.org/10.1007/s00432-022-04011-3