Proteomics Studies on Extracellular Vesicles Derived from Glioblastoma: Where Do We Stand?
Abstract
:1. Introduction
2. Types of EVs and Methods to Isolate and Identify Them
3. Proteomics Applied to EVs from Various Sources
3.1. Techniques Used to Study the Proteomic Cargo of GBM-Derived EVs
3.2. Proteomics Applied to EVs Obtained from Cultured Cells
3.3. Proteomics Applied to EVs Obtained from Patients’ Biological Fluids
3.4. Proteomics Applied to EVs Obtained from Brain Tumors
4. Discussion and Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Eckerdt, F.; Platanias, L.C. Emerging Role of Glioma Stem Cells in Mechanisms of Therapy Resistance. Cancers 2023, 15, 3458. [Google Scholar] [CrossRef] [PubMed]
- Verdugo, E.; Puerto, I.; Medina, M.Á. An update on the molecular biology of glioblastoma, with clinical implications and progress in its treatment. Cancer Commun. 2022, 42, 1083–1111. [Google Scholar] [CrossRef] [PubMed]
- Virtuoso, A.; D’Amico, G.; Scalia, F.; De Luca, C.; Papa, M.; Maugeri, G.; D’Agata, V.; Caruso Bavisotto, C.; D’Amico, A.G. The Interplay between Glioblastoma Cells and Tumor Microenvironment: New Perspectives for Early Diagnosis and Targeted Cancer Therapy. Brain Sci. 2024, 14, 331. [Google Scholar] [CrossRef] [PubMed]
- Matarredona, E.R.; Pastor, A.M. Extracellular vesicle-mediated communication between the glioblastoma and its microenvironment. Cells 2019, 9, 96. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Graner, A.N.; Knowles, B.; McRae, C.; Fringuello, A.; Paucek, P.; Gavrilovic, M.; Redwine, M.; Hanson, C.; Coughlan, C.; et al. A tale of two tumors: Differential, but detrimental, effects of glioblastoma extracellular vesicles (EVs) on normal human brain cells. bioRxiv 2024. [Google Scholar] [CrossRef]
- Shahi, S.; Kang, T.; Fonseka, P. Extracellular Vesicles in Pathophysiology: A Prudent Target That Requires Careful Consideration. Cells 2024, 13, 754. [Google Scholar] [CrossRef]
- Simon, T.; Jackson, E.; Giamas, G. Breaking through the glioblastoma micro-environment via extracellular vesicles. Oncogene 2020, 39, 4477–4490. [Google Scholar] [CrossRef]
- Dai, J.; Jiang, Y.; Hu, H.; Zhang, S.; Chen, Y. Extracellular vesicles as modulators of glioblastoma progression and tumor microenvironment. Pathol. Oncol. Res. 2024, 30, 1611549. [Google Scholar] [CrossRef]
- Russo, M.N.; Whaley, L.A.; Norton, E.S.; Zarco, N.; Guerrero-Cázares, H. Extracellular vesicles in the glioblastoma microenvironment: A diagnostic and therapeutic perspective. Mol. Aspects Med. 2023, 91, 101167. [Google Scholar] [CrossRef]
- Bertolini, I.; Terrasi, A.; Martelli, C.; Gaudioso, G.; Di Cristofori, A.; Storaci, A.M.; Formica, M.; Braidotti, P.; Todoerti, K.; Ferrero, S.; et al. A GBM-like V-ATPase signature directs cell-cell tumor signaling and reprogramming via large oncosomes. EBioMedicine 2019, 41, 225–235. [Google Scholar] [CrossRef]
- Liu, Y.J.; Wang, C. A review of the regulatory mechanisms of extracellular vesicles-mediated intercellular communication. Cell Commun. Signal. 2023, 21, 77. [Google Scholar] [CrossRef] [PubMed]
- Ciardiello, C.; Migliorino, R.; Leone, A.; Budillon, A. Large extracellular vesicles: Size matters in tumor progression. Cytokine Growth Factor Rev. 2020, 51, 69–74. [Google Scholar] [CrossRef] [PubMed]
- Del Bene, M.; Osti, D.; Faletti, S.; Beznoussenko, G.V.; DiMeco, F.; Pelicci, G. Extracellular vesicles: The key for precision medicine in glioblastoma. Neuro-Oncology 2022, 24, 184–196. [Google Scholar] [CrossRef] [PubMed]
- Vaiaki, E.M.; Falasca, M. Comparative analysis of the minimal information for studies of extracellular vesicles guidelines: Advancements and implications for extracellular vesicle research. Semin. Cancer Biol. 2024, 101, 12–24. [Google Scholar] [CrossRef] [PubMed]
- Roda, D.; Veiga, P.; Melo, J.B.; Carreira, I.M.; Ribeiro, I.P. Principles in the Management of Glioblastoma. Genes 2024, 15, 501. [Google Scholar] [CrossRef]
- Hoggarth, A.R.; Muthukumar, S.; Thomas, S.M.; Crowley, J.; Kiser, J.; Witcher, M.R. Clinical Theranostics in Recurrent Gliomas: A Review. Cancers 2024, 16, 1715. [Google Scholar] [CrossRef]
- Yekula, A.; Yekula, A.; Muralidharan, K.; Kang, K.; Carter, B.S.; Balaj, L. Extracellular Vesicles in Glioblastoma Tumor Microenvironment. Front. Immunol. 2020, 10, 3137. [Google Scholar] [CrossRef]
- Hosseini, A.; Ashraf, H.; Rahimi, F.; Alipourfard, I.; Alivirdiloo, V.; Hashemi, B.; Yazdani, Y.; Ghazi, F.; Eslami, M.; Ameri Shah Reza, M.; et al. Recent advances in the detection of glioblastoma.; from imaging-based methods to proteomics and biosensors: A narrative review. Cancer Cell Int. 2023, 23, 98. [Google Scholar] [CrossRef]
- Cumba Garcia, L.M.; Bouchal, S.M.; Bauman, M.M.J.; Parney, I.F. Advancements and Technical Considerations for Extracellular Vesicle Isolation and Biomarker Identification in Glioblastoma. Neurosurgery 2023, 93, 33–42. [Google Scholar] [CrossRef]
- Mukherjee, S.; Pillai, P.P. Current insights on extracellular vesicle-mediated glioblastoma progression: Implications in drug resistance and epithelial-mesenchymal transition. Biochim. Biophys. Acta Gen. Subj. 2022, 1866, 130065. [Google Scholar] [CrossRef]
- Adhit, K.K.; Wanjari, A.; Menon, S.; Siddhaarth, K. Liquid Biopsy: An Evolving Paradigm for Non-invasive Disease Diagnosis and Monitoring in Medicine. Cureus 2023, 15, e50176. [Google Scholar] [CrossRef] [PubMed]
- Bauman, M.M.J.; Bouchal, S.M.; Monie, D.D.; Aibaidula, A.; Singh, R.; Parney, I.F. Strategies, considerations, and recent advancements in the development of liquid biopsy for glioblastoma: A step towards individualized medicine in glioblastoma. Neurosurg. Focus 2022, 53, E14. [Google Scholar] [CrossRef] [PubMed]
- Di Sario, G.; Rossella, V.; Famulari, E.S.; Maurizio, A.; Lazarevic, D.; Giannese, F.; Felici, C. Enhancing clinical potential of liquid biopsy through a multi-omic approach: A systematic review. Front. Genet. 2023, 14, 1152470. [Google Scholar] [CrossRef]
- Heidarzadeh, M.; Zarebkohan, A.; Rahbarghazi, R.; Sokullu, E. Protein corona and exosomes: New challenges and prospects. Cell Commun. Signal. 2023, 21, 64. [Google Scholar] [CrossRef]
- Wolf, M.; Poupardin, R.W.; Ebner-Peking, P.; Andrade, A.C.; Blöchl, C.; Obermayer, A.; Gomes, F.G.; Vari, B.; Maeding, N.; Eminger, E.; et al. A functional corona around extracellular vesicles enhances angiogenesis, skin regeneration and immunomodulation. J. Extracell. Vesicles 2022, 11, e12207. [Google Scholar] [CrossRef]
- Chhoy, P.; Brown, C.W.; Amante, J.J.; Mercurio, A.M. Protocol for the separation of extracellular vesicles by ultracentrifugation from in vitro cell culture models. STAR Protoc. 2021, 2, 100303. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Jeppesen, D.K.; Higginbotham, N.; Franklin, J.L.; Coffey, R.J. Comprehensive isolation of extracellular vesicles and nanoparticles. Nat. Protoc. 2023, 18, 1462–1487. [Google Scholar] [CrossRef]
- Kang, H.; Kim, J.; Park, J. Methods to isolate extracellular vesicles for diagnosis. Micro Nano Syst. Lett. 2017, 5, 15. [Google Scholar] [CrossRef]
- Wang, W.; Sun, H.; Duan, H.; Sheng, G.; Tian, N.; Liu, D.; Sun, Z. Isolation and usage of exosomes in central nervous system diseases. CNS Neurosci. Ther. 2024, 30, e14677. [Google Scholar] [CrossRef] [PubMed]
- Whitesides, G.M. The Origins and the Future of Microfluidics. Nature 2006, 442, 368–373. [Google Scholar] [CrossRef]
- Jalali, M.; Isaac Hosseini, I.; AbdelFatah, T.; Montermini, L.; Wachsmann Hogiu, S.; Rak, J.; Mahshid, S. Plasmonic nanobowtiefluidic device for sensitive detection of glioma extracellular vesicles by Raman spectrometry. Lab Chip 2021, 21, 855–866. [Google Scholar] [CrossRef] [PubMed]
- Jalali, M.; Del Real Mata, C.; Montermini, L.; Jeanne, O.; Hosseini, I.; Gu, Z.; Spinelli, C.; Lu, Y.; Tawil, N.; Guiot, M.C.; et al. MoS2-Plasmonic Nanocavities for Raman Spectra of Single Extracellular Vesicles Reveal Molecular Progression in Glioblastoma. ACS Nano 2023, 17, 12052–12071. [Google Scholar] [CrossRef] [PubMed]
- Meggiolaro, A.; Moccia, V.; Brun, P.; Pierno, M.; Mistura, G.; Zappulli, V.; Ferraro, D. Microfluidic Strategies for Extracellular Vesicle Isolation: Towards Clinical Applications. Biosensors 2022, 13, 50. [Google Scholar] [CrossRef] [PubMed]
- Havers, M.; Broman, A.; Lenshof, A.; Laurell, T. Advancement and obstacles in microfluidics-based isolation of extracellular vesicles. Anal. Bioanal. Chem. 2023, 415, 1265–1285. [Google Scholar] [CrossRef]
- Zhu, L.; Tian, W.; Yuan, L.; Chi, C.; Wang, Y.; Xiao, Q.; Zheng, M.; Yang, C.; Song, Y. Aptamer-based extracellular vesicle isolation, analysis and therapeutics. Interdiscip. Med. 2023, 1, e20220019. [Google Scholar] [CrossRef]
- Chrimes, A.F.; Khoshmanesh, K.; Stoddart, P.R.; Mitchell, A.; Kalantar-Zadeh, K. Microfluidics and Raman microscopy: Current applications and future challenges. Chem. Soc. Rev. 2013, 42, 5880–5906. [Google Scholar] [CrossRef]
- Welsh, J.A.; Goberdhan, D.C.I.; O’Driscoll, L.; Buzas, E.I.; Blenkiron, C.; Bussolati, B.; Cai, H.; Di Vizio, D.; Driedonks, T.A.P.; Erdbrügger, U.; et al. Minimal information for studies of extracellular vesicles (MISEV2023): From basic to advanced approaches. J. Extracell. Vesicles 2024, 13, e12404, Erratum in J. Extracell. Vesicles 2024, 13, e12451. [Google Scholar] [CrossRef]
- Malenica, M.; Vukomanović, M.; Kurtjak, M.; Masciotti, V.; Dal Zilio, S.; Greco, S.; Lazzarino, M.; Krušić, V.; Perčić, M.; Jelovica Badovinac, I.; et al. Perspectives of Microscopy Methods for Morphology Characterisation of Extracellular Vesicles from Human Biofluids. Biomedicines 2021, 9, 603. [Google Scholar] [CrossRef]
- Szatanek, R.; Baj-Krzyworzeka, M.; Zimoch, J.; Lekka, M.; Siedlar, M.; Baran, J. The methods of choice for extracellular vesicles (EVs) characterization. Int. J. Mol. Sci. 2017, 18, 1153. [Google Scholar] [CrossRef]
- Soo, C.Y.; Song, Y.; Zheng, Y.; Campbell, E.C.; Riches, A.C.; Gunn-Moore, F.; Powis, S.J. Nanoparticle tracking analysis monitors microvesicle and exosome secretion from immune cells. Immunology 2012, 136, 192–197. [Google Scholar] [CrossRef]
- Webber, J.; Clayton, A. How pure are your vesicles? J. Extracell. Vesicles 2013, 2, 19861. [Google Scholar] [CrossRef] [PubMed]
- Willmott, G.R. Tunable Resistive Pulse Sensing: Better Size and Charge Measurements for Submicrometer Colloids. Anal. Chem. 2018, 90, 2987–2995. [Google Scholar] [CrossRef] [PubMed]
- Orozco, A.F.; Lewis, D.E. Flow cytometric analysis of circulating microparticles in plasma. Cytom. Part A 2010, 77, 502–514. [Google Scholar] [CrossRef] [PubMed]
- Van Der Pol, E.; van Gemert, M.J.; Sturk, A.; Nieuwland, R.; van Leeuwen, T.G. Single vs. swarm detection of microparticles and exosomes by flow cytometry. J. Thromb. Haemost. 2012, 10, 919–930. [Google Scholar] [CrossRef]
- Franquesa, M.; Hoogduijn, M.J.; Ripoll, E.; Luk, F.; Salih, M.; Betjes, M.G.; Torras, J.; Baan, C.C.; Grinyó, J.M.; Merino, A.M. Update on controls for isolation and quantification methodology of extracellular vesicles derived from adipose tissue mesenchymal stem cells. Front. Immunol. 2014, 5, 525. [Google Scholar] [CrossRef]
- Hartjes, T.A.; Mytnyk, S.; Jenster, G.W.; van Steijn, V.; van Royen, M.E. Extracellular Vesicle Quantification and Characterization: Common Methods and Emerging Approaches. Bioengineering 2019, 6, 7. [Google Scholar] [CrossRef]
- Pisitkun, T.; Shen, R.F.; Knepper, M.A. Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. USA 2004, 101, 13368–13373. [Google Scholar] [CrossRef]
- Chiang, C.Y.; Chen, C. Toward characterizing extracellular vesicles at a single-particle level. J. Biomed. Sci. 2019, 26, 9. [Google Scholar] [CrossRef]
- Zhao, Z.; Wijerathne, H.; Godwin, A.K.; Soper, S.A. Isolation and analysis methods of extracellular vesicles (EVs). Extracell. Vesicles Circ. Nucleic Acids 2021, 2, 80–103. [Google Scholar] [CrossRef]
- Cancer Genome Atlas Research Network. Comprehensive Genomic Characterization Defines Human Glioblastoma Genes and Core Pathways. Nature 2008, 455, 1061–1068. [Google Scholar] [CrossRef]
- Iyer, K.; Saini, S.; Bhadra, S.; Kulavi, S.; Bandyopadhyay, J. Precision medicine advancements in glioblastoma: A systematic review. Biomedicine 2023, 13, 1–13. [Google Scholar] [CrossRef]
- Louis, D.N.; Perry, A.; Reifenberger, G.; von Deimling, A.; Figarella-Branger, D.; Cavenee, W.K.; Ohgaki, H.; Wiestler, O.D.; Kleihues, P.; Ellison, D.W. The 2016 World Health Organization Classification of Tumors of the Central Nervous System: A Summary. Acta Neuropathol. 2016, 131, 803–820. [Google Scholar] [CrossRef] [PubMed]
- Wu, L.; Candille, S.I.; Choi, Y.; Xie, D.; Jiang, L.; Li-Pook-Than, J.; Tang, H.; Snyder, M. Variation and genetic control of protein abundance in humans. Nature 2013, 499, 79–82. [Google Scholar] [CrossRef] [PubMed]
- Chheda, U.; Pradeepan, S.; Esposito, E.; Strezsak, S.; Fernandez-Delgado, O.; Kranz, J. Factors Affecting Stability of RNA—Temperature, Length, Concentration, pH, and Buffering Species. J. Pharm. Sci. 2024, 113, 377–385. [Google Scholar] [CrossRef] [PubMed]
- Xue, V.W.; Yang, C.; Wong, S.C.C.; Cho, W.C.S. Proteomic profiling in extracellular vesicles for cancer detection and monitoring. Proteomics 2021, 21, e2000094. [Google Scholar] [CrossRef]
- Silantyev, A.; Falzone, L.; Libra, M.; Gurina, O.; Kardashova, K.; Nikolouzakis, T.; Nosyrev, A.; Sutton, C.; Mitsias, P.; Tsatsakis, A. Current and Future Trends on Diagnosis and Prognosis of Glioblastoma: From Molecular Biology to Proteomics. Cells 2019, 8, 863. [Google Scholar] [CrossRef]
- La Rocca, G.; Simboli, G.A.; Vincenzoni, F.; Rossetti, D.V.; Urbani, A.; Ius, T.; Della Pepa, G.M.; Olivi, A.; Sabatino, G.; Desiderio, C. Glioblastoma Cusa Fluid Protein Profiling: A Comparative Investigation of the Core and Peripheral Tumor Zones. Cancers 2021, 13, 30. [Google Scholar] [CrossRef]
- Tribe, A.K.W.; McConnell, M.J.; Teesdale-Spittle, P.H. The Big Picture of Glioblastoma Malignancy: A Meta-Analysis of Glioblastoma Proteomics to Identify Altered Biological Pathways. ACS Omega 2021, 6, 24535–24544. [Google Scholar] [CrossRef]
- Meier, F.; Park, M.A.; Mann, M. Trapped Ion Mobility Spectrometry and Parallel Accumulation-Serial Fragmentation in Proteomics. Mol. Cell. Proteom. 2021, 20, 100138. [Google Scholar] [CrossRef]
- Naylor, C.N.; Nagy, G. Recent advances in high-resolution traveling wave-based ion mobility separations coupled to mass spectrometry. Mass Spectrom. Rev. 2024. early view. [Google Scholar] [CrossRef]
- Vasilopoulou, C.G.; Sulek, K.; Brunner, A.D.; Meitei, N.S.; Schweiger-Hufnagel, U.; Meyer, S.W.; Barsch, A.; Mann, M.; Meier, F. Trapped ion mobility spectrometry and PASEF enable in-depth lipidomics from minimal sample amounts. Nat. Commun. 2020, 11, 331. [Google Scholar] [CrossRef] [PubMed]
- Bichmann, L.; Gupta, S.; Rosenberger, G.; Kuchenbecker, L.; Sachsenberg, T.; Ewels, P.; Alka, O.; Pfeuffer, J.; Kohlbacher, O.; Röst, H. DIA proteomics: A Multifunctional Data Analysis Pipeline for Data-Independent Acquisition Proteomics and Peptidomics. J. Proteome Res. 2021, 20, 3758–3766. [Google Scholar] [CrossRef]
- Carrillo-Rodriguez, P.; Selheim, F.; Hernandez-Valladares, M. Mass Spectrometry-Based Proteomics Workflows in Cancer Research: The Relevance of Choosing the Right Steps. Cancers 2023, 15, 555. [Google Scholar] [CrossRef]
- Cross, J.; Rai, A.; Fang, H.; Claridge, B.; Greening, D.W. Rapid and in-depth proteomic profiling of small extracellular vesicles for ultralow samples. Proteomics 2024, 24, e2300211. [Google Scholar] [CrossRef] [PubMed]
- Lou, R.; Shui, W. Acquisition and Analysis of DIA-Based Proteomic Data: A Comprehensive Survey in 2023. Mol. Cell. Proteom. 2024, 23, 100712. [Google Scholar] [CrossRef] [PubMed]
- Schubert, O.T.; Gillet, L.C.; Collins, B.C.; Navarro, P.; Rosenberger, G.; Wolski, W.E.; Lam, H.; Amodei, D.; Mallick, P.; MacLean, B.; et al. Building high-quality assay libraries for targeted analysis of SWATH MS data. Nat. Protoc. 2015, 10, 426–441. [Google Scholar] [CrossRef] [PubMed]
- Dupree, E.J.; Jayathirtha, M.; Yorkey, H.; Mihasan, M.; Petre, B.A.; Darie, C.C. A Critical Review of Bottom-Up Proteomics: The Good, the Bad, and the Future of This Field. Proteomes 2020, 8, 14. [Google Scholar] [CrossRef]
- Graner, M.W.; Cumming, R.I.; Bigner, D.D. The heat shock response and chaperones/heat shock proteins in brain tumors: Surface expression, release, and possible immune consequences. J. Neurosci. 2007, 27, 11214–11227. [Google Scholar] [CrossRef]
- Scholl, J.N.; de Fraga Dias, A.; Pizzato, P.R.; Lopes, D.V.; Moritz, C.E.J.; Jandrey, E.H.F.; Souto, G.D.; Colombo, M.; Rohden, F.; Sévigny, J.; et al. Characterization and antiproliferative activity of glioma-derived extracellular vesicles. Nanomedicine 2020, 15, 1001–1018. [Google Scholar] [CrossRef]
- Panzarini, E.; Tacconi, S.; Carata, E.; Mariano, S.; Tata, A.M.; Dini, L. Molecular Characterization of Temozolomide-Treated and Non Temozolomide-Treated Glioblastoma Cells Released Extracellular Vesicles and Their Role in the Macrophage Response. Int. J. Mol. Sci. 2020, 21, 8353. [Google Scholar] [CrossRef]
- Kıyga, E.; Adıgüzel, Z.; Önay Uçar, E. Temozolomide increases heat shock proteins in extracellular vesicles released from glioblastoma cells. Mol. Biol. Rep. 2022, 49, 8701–8713. [Google Scholar] [CrossRef]
- Graner, M.W.; Alzate, O.; Dechkovskaia, A.M.; Keene, J.D.; Sampson, J.H.; Mitchell, D.A.; Bigner, D.D. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009, 23, 1541–1557. [Google Scholar] [CrossRef]
- Shao, H.; Chung, J.; Balaj, L.; Charest, A.; Bigner, D.D.; Carter, B.S.; Hochberg, F.H.; Breakefield, X.O.; Weissleder, R.; Lee, H. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat. Med. 2012, 18, 1835–1840. [Google Scholar] [CrossRef]
- Mallawaaratchy, D.M.; Hallal, S.; Russell, B.; Ly, L.; Ebrahimkhani, S.; Wei, H.; Christopherson, R.I.; Buckland, M.E.; Kaufman, K.L. Comprehensive proteome profiling of glioblastoma-derived extracellular vesicles identifies markers for more aggressive disease. J. Neurooncol. 2017, 131, 233–244. [Google Scholar] [CrossRef]
- Whitehead, C.A.; Fang, H.; Su, H.; Morokoff, A.P.; Kaye, A.H.; Hanssen, E.; Nowell, C.J.; Drummond, K.J.; Greening, D.W.; Vella, L.J.; et al. Small extracellular vesicles promote invadopodia activity in glioblastoma cells in a therapy-dependent manner. Cell. Oncol. 2023, 46, 909–931. [Google Scholar] [CrossRef]
- Choi, D.; Montermini, L.; Kim, D.K.; Meehan, B.; Roth, F.P.; Rak, J. The Impact of Oncogenic EGFRvIII on the Proteome of Extracellular Vesicles Released from Glioblastoma Cells. Mol. Cell. Proteom. 2018, 17, 1948–1964. [Google Scholar] [CrossRef]
- Naryzhny, S.; Volnitskiy, A.; Kopylov, A.; Zorina, E.; Kamyshinsky, R.; Bairamukov, V.; Garaeva, L.; Shlikht, A.; Shtam, T. Proteome of Glioblastoma-Derived Exosomes as a Source of Biomarkers. Biomedicines 2020, 8, 216. [Google Scholar] [CrossRef]
- Théry, C.; Witwer, K.W.; Aikawa, E.; Alcaraz, M.J.; Anderson, J.D.; Andriantsitohaina, R.; Antoniou, A.; Arab, T.; Archer, F.; Atkin-Smith, G.K.; et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles 2018, 7, 1535750. [Google Scholar] [CrossRef]
- Di Giuseppe, F.; Carluccio, M.; Zuccarini, M.; Giuliani, P.; Ricci-Vitiani, L.; Pallini, R.; De Sanctis, P.; Di Pietro, R.; Ciccarelli, R.; Angelucci, S. Proteomic Characterization of Two Extracellular Vesicle Subtypes Isolated from Human Glioblastoma Stem Cell Secretome by Sequential Centrifugal Ultrafiltration. Biomedicines 2021, 9, 146. [Google Scholar] [CrossRef]
- Lane, R.; Simon, T.; Vintu, M.; Solkin, B.; Koch, B.; Stewart, N.; Benstead-Hume, G.; Pearl, F.M.G.; Critchley, G.; Stebbing, J.; et al. Cell-derived extracellular vesicles can be used as a biomarker reservoir for glioblastoma tumor subtyping. Commun. Biol. 2019, 2, 315. [Google Scholar] [CrossRef]
- Rocha, C.R.; Kajitani, G.S.; Quinet, A.; Fortunato, R.S.; Menck, C.F. NRF2 and glutathione are key resistance mediators to temozolomide in glioma and melanoma cells. Oncotarget 2016, 7, 48081–48092. [Google Scholar] [CrossRef] [PubMed]
- Di Giuseppe, F.; Ricci-Vitiani, L.; Pallini, R.; Di Pietro, R.; Di Iorio, P.; Ascani, G.; Ciccarelli, R.; Angelucci, S. Changes Induced by P2X7 Receptor Stimulation of Human Glioblastoma Stem Cells in the Proteome of Extracellular Vesicles Isolated from Their Secretome. Cells 2024, 13, 571. [Google Scholar] [CrossRef] [PubMed]
- Adinolfi, E.; De Marchi, E.; Grignolo, M.; Szymczak, B.; Pegoraro, A. The P2X7 Receptor in Oncogenesis and Metastatic Dissemination: New Insights on Vesicular Release and Adenosinergic Crosstalk. Int. J. Mol. Sci. 2023, 24, 13906. [Google Scholar] [CrossRef]
- Cifola, I.; Fratini, F.; Cardinali, B.; Palmieri, V.; Gatti, G.; Selmi, T.; Donzelli, S.; Sacconi, A.; Cesarini, V.; Marei, H.E.; et al. miRNome and Proteome Profiling of Small Extracellular Vesicles Secreted by Human Glioblastoma Cell Lines and Primary Cancer Stem Cells. Biomedicines 2022, 10, 1886. [Google Scholar] [CrossRef] [PubMed]
- Miyauchi, E.; Furuta, T.; Ohtsuki, S.; Tachikawa, M.; Uchida, Y.; Sabit, H.; Obuchi, W.; Baba, T.; Watanabe, M.; Terasaki, T.; et al. Identification of Blood Biomarkers in Glioblastoma by SWATH Mass Spectrometry and Quantitative Targeted Absolute Proteomics. PLoS ONE. 2018, 13, e0193799. [Google Scholar] [CrossRef]
- Skouras, P.; Markouli, M.; Kalamatianos, T.; Stranjalis, G.; Korkolopoulou, P.; Piperi, C. Advances on Liquid Biopsy Analysis for Glioma Diagnosis. Biomedicines 2023, 11, 2371. [Google Scholar] [CrossRef]
- Zanganeh, S.; Abbasgholinejad, E.; Doroudian, M.; Esmaelizad, N.; Farjadian, F.; Benhabbour, S.R. The Current Landscape of Glioblastoma Biomarkers in Body Fluids. Cancers 2023, 15, 3804. [Google Scholar] [CrossRef]
- Shen, F.; Zhang, Y.; Yao, Y.; Hua, W.; Zhang, H.S.; Wu, J.S.; Zhong, P.; Zhou, L.F. Proteomic analysis of cerebrospinal fluid: Toward the identification of biomarkers for gliomas. Neurosurg. Rev. 2014, 37, 367–380. [Google Scholar] [CrossRef]
- Valerius, A.R.; Webb, M.J.; Hammad, N.; Sener, U.; Malani, R. Cerebrospinal Fluid Liquid Biopsies in the Evaluation of Adult Gliomas. Curr. Oncol. Rep. 2024, 26, 377–3390. [Google Scholar] [CrossRef]
- Papadimitrakis, D.; Perdikakis, M.; Gargalionis, A.N.; Papavassiliou, A.G. Biomarkers in Cerebrospinal Fluid for the Diagnosis and Monitoring of Gliomas. Biomolecules 2024, 14, 801. [Google Scholar] [CrossRef]
- Greco, F.; Anastasi, F.; Pardini, L.F.; Dilillo, M.; Vannini, E.; Baroncelli, L.; Caleo, M.; McDonnell, L.A. Longitudinal Bottom-Up Proteomics of Serum, Serum Extracellular Vesicles, and Cerebrospinal Fluid Reveals Candidate Biomarkers for Early Detection of Glioblastoma in a Murine Model. Molecules 2021, 26, 5992. [Google Scholar] [CrossRef] [PubMed]
- Osti, D.; Del Bene, M.; Rappa, G.; Santos, M.; Matafora, V.; Richichi, C.; Faletti, S.; Beznoussenko, G.V.; Mironov, A.; Bachi, A.; et al. Clinical Significance of Extracellular Vesicles in Plasma from Glioblastoma Patients. Clin. Cancer Res. 2019, 25, 266–276. [Google Scholar] [CrossRef] [PubMed]
- Cumba Garcia, L.M.; Peterson, T.E.; Cepeda, M.A.; Johnson, A.J.; Parney, I.F. Isolation and Analysis of Plasma-Derived Exosomes in Patients with Glioma. Front. Oncol. 2019, 9, 651. [Google Scholar] [CrossRef]
- Tzaridis, T.; Weller, J.; Bachurski, D.; Shakeri, F.; Schaub, C.; Hau, P.; Buness, A.; Schlegel, U.; Steinbach, J.P.; Seidel, C.; et al. A novel serum extracellular vesicle protein signature to monitor glioblastoma tumor progression. Int. J. Cancer 2023, 152, 308–319. [Google Scholar] [CrossRef]
- Sandau, U.S.; Magaña, S.M.; Costa, J.; Nolan, J.P.; Ikezu, T.; Vella, L.J.; Jackson, H.K.; Moreira, L.R.; Palacio, P.L.; Hill, A.F.; et al. International Society for Extracellular Vesicles Cerebrospinal Fluid Task Force. Recommendations for reproducibility of cerebrospinal fluid extracellular vesicle studies. J. Extracell. Vesicles 2024, 13, e12397. [Google Scholar] [CrossRef]
- Jafari, D.; Tiyuri, A.; Rezaei, E.; Moradi, Y.; Jafari, R.; Jokar Shoorijeh, F.; Barati, M. Diagnostic accuracy of cerebrospinal fluid and serum-isolated extracellular vesicles for glioblastoma: A systematic review and meta-analysis. Expert Rev. Mol. Diagn. 2020, 20, 1075–1085. [Google Scholar] [CrossRef] [PubMed]
- Figueroa, J.M.; Skog, J.; Akers, J.; Li, H.; Komotar, R.; Jensen, R.; Ringel, F.; Yang, I.; Kalkanis, S.; Thompson, R.; et al. Detection of wild-type EGFR amplification and EGFRvIII mutation in CSF-derived extracellular vesicles of glioblastoma patients. Neuro-Oncology 2017, 19, 1494–1502. [Google Scholar] [CrossRef]
- Skoczylas, Ł.; Gawin, M.; Fochtman, D.; Widłak, P.; Whiteside, T.L.; Pietrowska, M. Immune capture and protein profiling of small extracellular vesicles from human plasma. Proteomics 2024, 24, e2300180. [Google Scholar] [CrossRef]
- Indira Chandran, V.; Welinder, C.; Månsson, A.S.; Offer, S.; Freyhult, E.; Pernemalm, M.; Lund, S.M.; Pedersen, S.; Lehtiö, J.; Marko-Varga, G.; et al. Ultrasensitive Immunoprofiling of Plasma Extracellular Vesicles Identifies Syndecan-1 as a Potential Tool for Minimally Invasive Diagnosis of Glioma. Clin. Cancer Res. 2019, 25, 3115–3127. [Google Scholar] [CrossRef]
- Hallal, S.; Azimi, A.; Wei, H.; Ho, N.; Lee, M.Y.T.; Sim, H.W.; Sy, J.; Shivalingam, B.; Buckland, M.E.; Alexander-Kaufman, K.L. A Comprehensive Proteomic SWATH-MS Workflow for Profiling Blood Extracellular Vesicles: A New Avenue for Glioma Tumour Surveillance. Int. J. Mol. Sci. 2020, 21, 4754. [Google Scholar] [CrossRef]
- Cilibrasi, C.; Simon, T.; Vintu, M.; Tolias, C.; Samuels, M.; Mazarakis, N.K.; Eravci, M.; Stewart, N.; Critchley, G.; Giamas, G. Definition of an inflammatory biomarker signature in plasma-derived extracellular vesicles of glioblastoma patients. Biomedicines 2022, 10, 125. [Google Scholar] [CrossRef] [PubMed]
- Katsani, K.R.; Sakellari, D. Saliva proteomics updates in biomedicine. J. Biol. Res. 2019, 26, 17. [Google Scholar] [CrossRef]
- Han, Y.; Jia, L.; Zheng, Y.; Li, W. Salivary exosomes: Emerging roles in systemic disease. Int. J. Biol. Sci. 2018, 14, 633–643. [Google Scholar] [CrossRef]
- Tang, K.D.; Wan, Y.; Zhang, X.; Bozyk, N.; Vasani, S.; Kenny, L.; Punyadeera, C. Proteomic alterations in salivary exosomes derived from human papillomavirus-driven oropharyngeal cancer. Mol. Diagn. Ther. 2021, 25, 505–515. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Huo, C.; Qiao, Z.; Shang, Z.; Uzzaman, A.; Liu, S.; Jiang, X.; Fan, L.Y.; Ji, L.; Guan, X.; et al. Comparative proteomic analysis of exosomes and microvesicles in human saliva for lung cancer. J. Proteome Res. 2018, 17, 1101–1107. [Google Scholar] [CrossRef]
- Müller Bark, J.; Trevisan França de Lima, L.; Zhang, X.; Broszczak, D.; Leo, P.J.; Jeffree, R.L.; Chua, B.; Day, B.W.; Punyadeera, C. Proteome profiling of salivary small extracellular vesicles in glioblastoma patients. Cancer 2023, 129, 2836–2847. [Google Scholar] [CrossRef] [PubMed]
- Hallal, S.M.; Tűzesi, Á.; Sida, L.A.; Xian, E.; Madani, D.; Muralidharan, K.; Shivalingam, B.; Buckland, M.E.; Satgunaseelan, L.; Alexander, K.L. Glioblastoma biomarkers in urinary extracellular vesicles reveal the potential for a ‘liquid gold’ biopsy. Br. J. Cancer 2024, 130, 836–851. [Google Scholar] [CrossRef]
- Su, H.; Purnianto, A.; Kaye, A.H.; Morokoff, A.P.; Drummond, K.J.; Stylly, S.; Vella, L.J. Proteome of human glioblastoma and meningioma tissue small extracellular vesicles. bioRxiv 2024. [Google Scholar] [CrossRef]
- Skog, J.; Wurdinger, T.; van Rijn, S.; Meijer, D.H.; Gainche, L.; Sena-Esteves, M.; Curry, W.T., Jr.; Carter, B.S.; Krichevsky, A.M.; Breakefield, X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10, 1470–1476. [Google Scholar] [CrossRef]
- Gabrusiewicz, K.; Li, X.; Wei, J.; Hashimoto, Y.; Marisetty, A.L.; Ott, M.; Wang, F.; Hawke, D.; Yu, J.; Healy, L.M.; et al. Glioblastoma stem cell-derived exosomes induce M2 macrophages and PD-L1 expression on human monocytes. Oncoimmunology 2018, 7, e1412909. [Google Scholar] [CrossRef]
- Ryskalin, L.; Biagioni, F.; Lenzi, P.; Frati, A.; Fornai, F. mTOR Modulates Intercellular Signals for Enlargement and Infiltration in Glioblastoma Multiforme. Cancers 2020, 12, 2486. [Google Scholar] [CrossRef] [PubMed]
- Romanò, S.; Nele, V.; Campani, V.; De Rosa, G.; Cinti, S. A comprehensive guide to extract information from extracellular vesicles: A tutorial review towards novel analytical developments. Anal. Chim. Acta 2024, 1302, 342473. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Zhou, X.; Kong, Q.; He, H.; Sun, J.; Qiu, W.; Zhang, L.; Yang, M. Extracellular Vesicle Preparation and Analysis: A State-of-the-Art Review. Adv. Sci. 2024, 11, e2401069. [Google Scholar] [CrossRef]
- Rufino-Ramos, D.; Lule, S.; Mahjoum, S.; Ughetto, S.; Cristopher Bragg, D.; Pereira de Almeida, L.; Breakefield, X.O.; Breyne, K. Using genetically modified extracellular vesicles as a non-invasive strategy to evaluate brain-specific cargo. Biomaterials 2022, 281, 121366. [Google Scholar] [CrossRef]
- Nakayasu, E.S.; Gritsenko, M.; Piehowski, P.D.; Gao, Y.; Orton, D.J.; Schepmoes, A.A.; Fillmore, T.L.; Frohnert, B.I.; Rewers, M.; Krischer, J.P.; et al. Tutorial: Best practices and considerations for mass-spectrometry-based protein biomarker discovery and validation. Nat. Protoc. 2021, 16, 3737–3760. [Google Scholar] [CrossRef]
- Metatla, I.; Roger, K.; Chhuon, C.; Ceccacci, S.; Chapelle, M.; Schmit, P.-O.; Demichev, V.; Guerrera, I.C. Neat plasma proteomics: Getting the best out of the worst. Clin. Proteom. 2024, 21, 22. [Google Scholar] [CrossRef]
- Holtz, A.; Basisty, N.; Schilling, B. Quantification and Identification of Post-Translational Modifications Using Modern Proteomics Approaches. Methods Mol. Biol. 2021, 2228, 225–235. [Google Scholar] [CrossRef] [PubMed]
- Brown, K.A.; Melby, J.A.; Roberts, D.S.; Ge, Y. Top-down proteomics: Challenges, innovations, and applications in basic and clinical research. Expert Rev. Proteom. 2020, 17, 719–733. [Google Scholar] [CrossRef] [PubMed]
- Coorssen, J.R.; Padula, M.P. Proteomics-The State of the Field: The Definition and Analysis of Proteomes Should Be Based in Reality, Not Convenience. Proteomes 2024, 12, 14. [Google Scholar] [CrossRef] [PubMed]
- Van Schaick, G.; Haselberg, R.; Somsen, G.W.; Wuhrer, M.; Domínguez-Vega, E. Studying protein structure and function by native separation-mass spectrometry. Nat. Rev. Chem. 2022, 6, 215–231. [Google Scholar] [CrossRef]
- Lin, T.T.; Zhang, T.; Kitata, R.B.; Liu, T.; Smith, R.D.; Qian, W.J.; Shi, T. Mass spectrometry-based targeted proteomics for analysis of protein mutations. Mass Spectrom. Rev. 2023, 42, 796–821. [Google Scholar] [CrossRef] [PubMed]
- Doll, S.; Gnad, F.; Mann, M. The Case for Proteomics and Phospho-Proteomics in Personalized Cancer Medicine. Proteom. Clin. Appl. 2019, 13, e1800113. [Google Scholar] [CrossRef]
- Chitluri, K.K.; Emerson, I.A. The importance of protein domain mutations in cancer therapy. Heliyon 2024, 10, e27655. [Google Scholar] [CrossRef] [PubMed]
- Ozaki, Y.; Broughton, P.; Abdollahi, H.; Valafar, H.; Blenda, A.V. Integrating Omics Data and AI for Cancer Diagnosis and Prognosis. Cancers 2024, 16, 2448. [Google Scholar] [CrossRef]
- Chen, M.; Lin, S.; Zhou, C.; Cui, D.; Haick, H.; Tang, N. From Conventional to Microfluidic: Progress in Extracellular Vesicle Separation and Individual Characterization. Adv. Healthc. Mater. 2023, 12, e2202437. [Google Scholar] [CrossRef]
- Zhang, Q.; Ren, T.; Cao, K.; Xu, Z. Advances of machine learning-assisted small extracellular vesicles detection strategy. Biosens. Bioelectron. 2024, 251, 116076. [Google Scholar] [CrossRef] [PubMed]
- Bamford, S.E.; Vassileff, N.; Spiers, J.G.; Gardner, W.; Winkler, D.A.; Muir, B.W.; Hill, A.F.; Pigram, P.J. High resolution imaging and analysis of extracellular vesicles using mass spectral imaging and machine learning. J. Extracell. Biol. 2023, 2, e110. [Google Scholar] [CrossRef]
- Rajczewski, A.T.; Jagtap, P.D.; Griffin, T.J. An overview of technologies for MS-based proteomics-centric multi-omics. Expert Rev. Proteom. 2022, 19, 165–181. [Google Scholar] [CrossRef]
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Microfluidic techniques (±optical or spectroscopic devices) using a
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Giuliani, P.; De Simone, C.; Febo, G.; Bellasame, A.; Tupone, N.; Di Virglio, V.; di Giuseppe, F.; Ciccarelli, R.; Di Iorio, P.; Angelucci, S. Proteomics Studies on Extracellular Vesicles Derived from Glioblastoma: Where Do We Stand? Int. J. Mol. Sci. 2024, 25, 9778. https://doi.org/10.3390/ijms25189778
Giuliani P, De Simone C, Febo G, Bellasame A, Tupone N, Di Virglio V, di Giuseppe F, Ciccarelli R, Di Iorio P, Angelucci S. Proteomics Studies on Extracellular Vesicles Derived from Glioblastoma: Where Do We Stand? International Journal of Molecular Sciences. 2024; 25(18):9778. https://doi.org/10.3390/ijms25189778
Chicago/Turabian StyleGiuliani, Patricia, Chiara De Simone, Giorgia Febo, Alessia Bellasame, Nicola Tupone, Vimal Di Virglio, Fabrizio di Giuseppe, Renata Ciccarelli, Patrizia Di Iorio, and Stefania Angelucci. 2024. "Proteomics Studies on Extracellular Vesicles Derived from Glioblastoma: Where Do We Stand?" International Journal of Molecular Sciences 25, no. 18: 9778. https://doi.org/10.3390/ijms25189778