Novel biomarker and drug delivery systems for theranostics - extracellular vesicles

• Autorzy: Stępień Ewa Ł. , Rząca Carina , Moskal Paweł

Identyfikatory

DOI

10.1515/bams-2021-0183

• Języki publikacji: EN

Abstrakty

EN

Extracellular vesicles (EVs) are nano- and micro-sized double-layered membrane entities derived from most cell types and released into biological fluids. Biological properties (cell-uptake, biocompatibility), and chemical (composition, structure) or physical (size, density) characteristics make EVs a good candidate for drug delivery systems (DDS). Recent advances in the field of EVs (e.g., scaling-up production, purification) and developments of new imaging methods (total-body positron emission tomography [PET]) revealed benefits of radiolabeled EVs in diagnostic and interventional medicine as a potential DDs in theranostics.

Słowa kluczowe

EN

biomarkers; DDS; exosomes; J-PET; positronium

• Wydawca: Uniwersytet Jagielloński - Collegium Medicum ; Index Copernicus Sp. z o.o.
• Czasopismo: Bio-Algorithms and Med-Systems
• Rocznik: 2021
• Tom: Vol. 17, no. 4
• Strony: 301--309
• Opis fizyczny: Bibliogr. 86 poz., rys.

Twórcy

autor

Stępień Ewa Ł.

• Instytut Fizyki im. Mariana Smoluchowskiego, Uniwersytet Jagielloński, 11 Łojasiewicza St., 30-348 Kraków, Poland
• Total-Body Jagiellonian-PET Laboratory, Jagiellonian University, Kraków, Poland
• Theranostics Center, Jagiellonian University, Kraków, Poland, Phone: [phone]

autor

Rząca Carina

• M. Smoluchowski Institute of Physics, Faculty of Physics, Astronomy and Applied Computer Science, Jagiellonian University, Krakow, Poland
• Theranostics Center, Jagiellonian University, Kraków, Poland

autor

Moskal Paweł

• M. Smoluchowski Institute of Physics, Faculty of Physics, Astronomy and Applied Computer Science, Jagiellonian University, Krakow, Poland
• Total-Body Jagiellonian-PET Laboratory, Jagiellonian University, Kraków, Poland
• Theranostics Center, Jagiellonian University, Kraków, Poland

• https://orcid.org/0000-0002-4229-3548

Bibliografia

• 1. Farquhar MG, Palade GE. Segregation of ferritin in glomerular protein absorption droplets. J Biophys Biochem Cytol 1960;7: 297-304.
• 2. Predescu SA, Predescu DN, Palade GE. Endothelial transcytotic machinery involves supramolecular protein-lipid complexes. Mol Biol Cell 2001;12:1019-33.
• 3. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967;13:269-88.
• 4. Kim DK, Lee J, Kim SR, Choi DS, Yoon YJ, Kim JH, et al. EVpedia: a community web portal for extracellular vesicles research. Bioinformatics 2015;1531:933-9.
• 5. Van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 2018;19:213-28.
• 6. Surman M, Drożdż A, Stępień E, Przybyło M. Extracellular vesicles as drug delivery systems - methods of production and potential therapeutic applications. Curr Pharmaceut Des 2019;25:132-54.
• 7. Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol 2015; 25:364-72.
• 8. Santavanond JP, Rutter SF, Atkin-Smith GK, Poon IKH. Apoptotic bodies: mechanism of formation, isolation and functional relevance. Subcell Biochem 2021;97:61-88.
• 9. Konkolewska M, Stępień E, Kurc S. A thousand words about microparticles in cardiology. J Med Sci 2014;2:189-93.
• 10. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999;94:3791-9.
• 11. Holme PA, Solum NO, Brosstad F, Egberg N, Lindahl TL. Stimulated Glanzmann’s thrombasthenia platelets produced microvesicles. Microvesiculation correlates better to exposure of procoagulant surface than to activation of GPIIb-IIIa. Thromb Haemostasis 1995;74:1533.
• 12. Thiagarajan P, Tait JF. Collagen-induced exposure of anionic phospholipid in platelets and platelet-derived microparticles. J Biol Chem 1991;266:24302.
• 13. Stępień E, Stankiewicz E, Zalewski J, Godlewski J, Zmudka K, Wybrańska I. Number of microparticles generated during acute myocardial infarction and stable angina correlates with platelet activation. Arch Med Res 2012;43:31-5.
• 14. Belniak-Legieć E, Stelmasiak Z. Blood platelet activation markers in patients with acute cerebral infarction during the earliest stage of the disease-evaluation using flow cytometry methods. Neurol Neurochir Pol 2000;34:853-64.
• 15. Stępień EŁ, Durak-Kozica M, Kamińska A, Targosz-Korecka M, Libera M, Tylko G, et al. Circulating ectosomes: determination of angiogenic microRNAs in type 2 diabetes. Theranostics 2018;8: 3874-90.
• 16. Omoto S, Nomura S, Shouzu A, Hayakawa T, Shimizu H, Miyake Y, et al. Significance of platelet-derived microparticles and activated platelets in diabetic nephropathy. Nephron 1999;81: 271-7.
• 17. Giró O, Jiménez A, Pané A, Badimon L, Ortega E, Chiva-Blanch G. Extracellular vesicles in atherothrombosis and cardiovascular disease: friends and foes. Atherosclerosis 2021;330:61-75.
• 18. Roman M, Kamińska A, Drożdż A, Platt M, Kuźniewski M, Małecki MT, et al. Raman spectral signatures of urinary extracellular vesicles from diabetic patients and hyperglycemic endothelial cells as potential biomarkers in diabetes. Nanomedicine 2019;17: 137-49.
• 19. Kamińska A, Roman M, Wróbel A, Gala-Błądzińska A, Małecki MT, Paluszkiewicz C, et al. Raman spectroscopy of urinary extracellular vesicles to stratify patients with chronic kidney disease in type 2 diabetes. Nanomedicine 2022;39:102468.
• 20. Aitekenov S, Gaipov A, Bukasov R. Review: detection and quantification of proteins in human urine. Talanta 2021;223: 121718.
• 21. Musante L, Tataruch D, Gu D, Liu X, Forsblom C, Groop PH, et al. Proteases and protease inhibitors of urinary extracellular vesicles in diabetic nephropathy. J Diabetes Res 2015;2015: 289734.
• 22. Tataruch-Weinert D, Musante L, Kretz O, Holthofer H. Urinary extracellular vesicles for RNA extraction: optimization of a protocol devoid of prokaryote contamination. J Extracell Vesicles 2016;5:30281.
• 23. Lytvyn Y, Xiao F, Kennedy CR, Perkins BA, Reich HN, Scholey JW, et al. Assessment of urinary microparticles in normotensive patients with type 1 diabetes. Diabetologia 2017;60: 581-4.
• 24. Erdbrügger U, Blijdorp CJ, Bijnsdorp IV, Borràs FE, Burger D, Bussolati B, et al. Urinary extracellular vesicles: a position paper by the urine task force of the International Society for Extracellular Vesicles. J Extracell Vesicles 2021;10:e12093.
• 25. Nilsson J, Skog J, Nordstrand A, Baranov V, Mincheva-Nilsson L, Breakefield XO, et al. Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. Br J Cancer 2009;100:1603-7.
• 26. Welton JL, Khanna S, Giles PJ, Brennan P, Brewis IA, Staffurth J, et al. Proteomics analysis of bladder cancer exosomes. Mol Cell Proteomics 2010;9:1324-38.
• 27. Wang W, Li H, Zhou Y, Jie S. Peripheral blood microvesicles are potential biomarkers for hepatocellular carcinoma. Cancer Biomarkers 2013;13:351-7.
• 28. Szabo G, Momen-Heravi F. Extracellular vesicles in liver disease and potential as biomarkers and therapeutic targets. Nat Rev Gastroenterol Hepatol 2017;14:455-66.
• 29. Yates KR, Welsh J, Echrish HH, Greenman J, Maraveyas A, Madden LA. Pancreatic cancer cell and microparticle procoagulant surface characterization: involvement of membrane-expressed tissue factor, phosphatidylserine and phosphatidylethanolamine. Blood Coagul Fibrinolysis 2011;22:680-7.
• 30. Yin L, Liu X, Shao X, Feng T, Xu J, Wang Q, et al. The role of exosomes in lung cancer metastasis and clinical applications: an updated review. J Transl Med 2021;19:312.
• 31. Periayah MH, Halim AS, Mat Saad AZ. Mechanism action of platelets and crucial blood coagulation pathways in hemostasis. Int J Hematol Oncol Stem Cell Res 2017;11:319-27.
• 32. Van Wijk MJ, Van Bavel E, Sturk A, Nieuwland R. Microparticles in cardiovascular diseases. Cardiovasc Res 2003;59:277-87.
• 33. Mause SF, Von Hundelshausen P, Zernecke A, Koenen RR, Weber C. Platelet microparticles: a transcellular delivery system for RANTES promoting monocyte recruitment on endothelium. Arterioscler Thromb Vasc Biol 2005;25:1512-8.
• 34. McGregor L, Martin J, McGregor JL. Platelet-leukocyte aggregates and derived microparticles in inflammation, vascular remodelling and thrombosis. Front Biosci 2006;11:830-7.
• 35. Chyrchel B, Drożdż A, Długosz D, Stępień EŁ, Surdacki A. Platelet reactivity and circulating platelet-derived microvesicles are differently affected by P2Y12 receptor antagonists. Int J Med Sci 2019;16:264-75.
• 36. Sekuła M, Janawa G, Stankiewicz E, Stępień E. Endothelial microparticle formation in moderate concentrations of homocysteine and methionine in vitro. Cell Mol Biol Lett 2011;16: 69-78.
• 37. Zhu J, Xie R, Piao X, Hou Y, Zhao C, Qiao G, et al. Homocysteine enhances clot-promoting activity of endothelial cells via phosphatidylserine externalization and microparticles formation. Amino Acids 2012;43:1243-50.
• 38. Sabatier F, Darmon P, Hugel B, Combes V, Sanmarco M, Velut JG, et al. Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes 2002;51:2840-5.
• 39. Kotb NA, Gaber R, Salah W, Elhendy A. Relations among glycemic control, circulating endothelial cells, nitric oxide, and flow mediated dilation in patients with type 2 diabetes mellitus. Exp Clin Endocrinol Diabetes 2012;120:460-5.
• 40. Li S, Wei J, Zhang C, Li X, Meng W, Mo X, et al. Cell-derived microparticles in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Cell Physiol Biochem 2016; 39:2439-50.
• 41. Nielsen MH, Irvine H, Vedel S, Raungaard B, Beck-Nielsen H, Handberg A. The impact of lipoprotein-associated oxidative stress on cell-specific microvesicle release in patients with familial hypercholesterolemia. Oxid Med Cell Longev 2016;2016: 2492858.
• 42. Lichtenauer M, Goebel B, Fritzenwanger M, Förster M, Betge S, Lauten A, et al. Simulated temporary hypoxia triggers the release of CD31+/Annexin+ endothelial microparticles: a prospective pilot study in humans. Clin Hemorheol Microcirc 2015;61:83-90.
• 43. Jia L, Fan J, Cui W, Liu S, Li N, Lau WB, et al. Endothelial cellderived microparticles from patients with obstructive sleep apnea hypoxia syndrome and coronary artery disease increase aortic endothelial cell dysfunction. Cell Physiol Biochem 2017; 43:2562-70.
• 44. Johnsen KB, Gudbergsson JM, Andresen TL, Simonsen JB. What is the blood concentration of extracellular vesicles? Implications for the use of extracellular vesicles as blood-borne biomarkers of cancer. Biochim Biophys Acta 2019;1871:109-16.
• 45. Available from: https://clinicaltrials.gov/ct2/home [Accessed 9 Nov 2021].
• 46. Available from: https://clinicaltrials.gov/ct2/show/study/ NCT04276987 [Accessed 9 Nov 2021].
• 47. Gąsecka A, Nieuwland R, Budnik M, Dignat-George F, Eyileten C, Harrison P, et al. Ticagrelor attenuates the increase of extracellular vesicle concentrations in plasma after acute myocardial infarction compared to clopidogrel. J Thromb Haemostasis 2020;18:609-23.
• 48. Tutrone R, Donovan MJ, Torkler P, Tadigotla V, McLain T, Noerholm M, et al. Clinical utility of the exosome based ExoDx Prostate (IntelliScore) EPI test in men presenting for initial Biopsy with a PSA 2-10 ng/mL. Prostate Cancer Prostatic Dis 2020;23: 607-14.
• 49. Vader P, Mol EA, Pasterkamp G, Schiffelers RM. Extracellular vesicles for drug delivery. Adv Drug Deliv Rev 2016;106:148-56.
• 50. Surman M, Hoja-Łukowicz D, Szwed S, Drożdż A, Stępień E, Przybyło M. Human melanoma-derived ectosomes are enriched with specific glycan epitopes. Life Sci 2018;207:395-411.
• 51. Andriessen A, Bongiovanni L, Driedonks TAP, van Liere E, Seijger A, Hegeman CV, et al. CDC6: a novel canine tumour biomarker detected in circulating extracellular vesicles. Vet Comp Oncol 2021;58:1476-5810.
• 52. Usynin IF, Dudarev AN, Miroshnichenko SM, Tkachenko TA, Gorodetskaya AY. Effect of native and modified apolipoprotein A-I on DNA synthesis in cultures of different cells. Bull Exp Biol Med 2017;164:247-51.
• 53. Surman M, Kędracka-Krok S, Hoja-Łukowicz D, Jankowska U, Drożdż A, Stępień EŁ, et al. Mass spectrometry-based proteomic characterization of cutaneous melanoma ectosomes reveals the presence of cancer-related molecules. Int J Mol Sci 2020;21:2934.
• 54. Tai CS, Chen YY, Chen WL. β-lactoglobulin influences human immunity and promotes cell proliferation. BioMed Res Int 2016; 2016:7123587.
• 55. Schneider AB, Edelhoch H. Equilibrium density centrifugation of thyroglobulin in RbCI: effect of iodine. J Biol Chem 1971;246: 6592-8.
• 56. Pintó RM, Ribes E, Jofre J, Bosch A. Retroviral properties inherent to viral erythrocytic infection in sea bass. Arch Virol 1995;140: 721-35.
• 57. Martin JF, Shaw T, Heggie J, Penington DG. Measurement of the density of human platelets and its relationship to volume. Br J Haematol 1983;54:337-52.
• 58. Langured T, Multia E, Riekkola ML. Modern isolation and separation techniques for extracellular vesicles. J Chromatogr A 2021;1636:461773.
• 59. Johnson J, Wu YW, Blyth C, Lichtfuss G, Goubran H, Burnouf T. Prospective therapeutic applications of platelet extracellular vesicles. Trends Biotechnol 2021;39:598-612.
• 60. Weiss J, Sauer A, Herzog M, Böger RH, Haefeli WE, Benndorf RA. Interaction of thiazolidinediones (glitazones) with the ATP-binding cassette transporters P-glycoprotein and breast cancer resistance protein. Pharmacology 2009;84:264-70.
• 61. Drożdż A, Kamińska A, Surman M, Gonet-Surówka A, Jach R, Huras H, et al. Low-vacuum filtration as an alternative extracellular vesicle concentration method: a comparison with ultracentrifugation and differential centrifugation. Pharmaceutics 2020;12:872.
• 62. Konoshenko MY, Lekchnov EA, Vlassov AV, Laktionov PP. Isolation of extracellular vesicles: general methodologies and latest trends. BioMed Res Int 2018;2018:8545347.
• 63. Talebjedi B, Tasnim N, Hoorfar M, Mastromonaco GF, Monteiro DE, Ferraz M. Exploiting microfluidics for extracellular vesicle isolation and characterization: potential use for standardized embryo quality assessment. Front Vet Sci 2021;7:620809.
• 64. Duong P, Chung A, Bouchareychas L, Raffai RL. Cushioneddensity gradient ultracentrifugation (C-DGUC) improves the isolation efficiency of extracellular vesicles. PLoS One 2019;14: e0215324.
• 65. Marsh SR, Pridham KJ, Jourdan J, Gourdie RG. Novel protocols for scalable production of high quality purified small extracellular vesicles from bovine milk. Nanotheranostics 2021;5:488-98.
• 66. Grangier A, Branchu J, Volatron J, Piffoux M, Gazeau F, Wilhelm C, et al. Technological advances towards extracellular vesicles mass production. Adv Drug Deliv Rev 2021;176:113843.
• 67. Guerreiro EM, Vestad B, Steffensen LA, Aass HCD, Saeed M, Øvstebø R, et al. Efficient extracellular vesicle isolation by combining cell media modifications, ultrafiltration, and size-exclusion chromatography. PLoS One 2018;13: e0204276.
• 68. Zhang C, Shang Y, Chen X, Midgley AC, Wang Z, Zhu D, et al. Supramolecular nanofibers containing arginine-glycineaspartate (RGD) peptides boost therapeutic efficacy of extracellular vesicles in kidney repair. ACS Nano 2020;14: 12133.
• 69. Kraińska MM, Pietrzkowska N, Turlej E, Zongjin L, Marycz K. Extracellular vesicles derived from mesenchymal stem cells as a potential therapeutic agent in acute kidney injury (AKI) in felines: review and perspectives. Stem Cell Res Ther 2021;12:504.
• 70. Mol EA, Lei Z, Roefs MT, Bakker MH, Goumans MJ, Doevendans PA, et al. Injectable supramolecular ureidopyrimidinone hydrogels provide sustained release of extracellular vesicle therapeutics. Adv Healthcare Mater 2019;8:1900847.
• 71. Moskal P, Stępień EŁ. Prospects and clinical perspectives of totalbody PET imaging using plastic scintillators. Pet Clin 2020;15: 439-52.
• 72. Vandenberghe S, Moskal P, Karp JS. State of the art in total body PET. EJNMMI Phys 2020;7:35.
• 73. Durak-Kozica M, Baster Z, Kubat K, Stępień E. 3D visualization of extracellular vesicle uptake by endothelial cells. Cell Mol Biol Lett 2018;23:57.
• 74. Alavi A, Reivich M. Guest editorial: the conception of FDG-PET imaging. Semin Nucl Med 2002;32:2-5.
• 75. Niedźwiecki S, Białas P, Curceanu C, Czerwiński E, Dulski K, Gajos A, et al. J-PET: a new technology for the whole-body PET imaging. Acta Phys Pol B 2017;48:1567.
• 76. Moskal P, Bednarski T, Niedźwiecki S, Silarski M, Czerwiński E, Kozik T, et al. Synchronization and calibration of the 24-modules J-PET prototype with 300-mm axial field of view. IEEE Trans Instrum Meas 2020;70:1-10.
• 77. Dulski K, Bass S, Chhokar J, Chug N, Curceanu C, Czerwiński E, et al. The J-PET detektor- a tool for precision studies of orthopositronium decays. Nucl Instrum Methods Phys Res, Sect A 2021;1008:165452.
• 78. Moskal P, Kisielewska D, Curceanu C, Czerwiński E, Dulski K, Gajos A, et al. Feasibility study of the positronium imaging with the J-PET tomograph. Phys Med Biol 2019;64:055017.
• 79. Moskal P, Gajos A, Mohammed M, Chhokar J, Chug N, Curceanu C, et al. Testing CPT symmetry in ortho-positronium decays with positronium annihilation tomography. Nat Commun 2021;12: 5658.
• 80. Choiński J, Łyczko M. Prospects for the production of radioisotopes and radio bioconjugates for Theranostics. Bio Algorithm Med Syst 2021;17:241-57.
• 81. Królicki L, Kunikowska J. Theranostics - present and future. Bio Algorithm Med Syst 2021;17:213-20.
• 82. Moskal P, Dulski K, Chug N, Curceanu C, Czerwiński E, Dadgar M, et al. Positronium imaging with the novel multiphoton PET scanner. Sci Adv 2021;7:eabh4394.
• 83. Moskal P, Jasińska B, Stępień EŁ, Bass SD. Positronium in medicine and biology. Nat Rev Phys 2019;1:527-9.
• 84. Khan AA, Rosales R. Radiolabelling of extracellular vesicles for PET and SPECT imaging. Nanotheranostics 2021;5:256-74.
• 85. Royo F, Cossío U, Ruiz de Angulo A, Llop J, Falcon-Perez JM. Modification of the glycosylation of extracellular vesicles alters their biodistribution in mice. Nanoscale 2019;11:1531-7.
• 86. Shi S, Li T, Wen X, Wu SY, Xiong C, Zhao J, et al. Copper-64 labeled PEGylated exosomes for in vivo positron emission tomography and enhanced tumor retention. Bioconjugate Chem 2019;30: 2675-83.

Uwagi

Opracowanie rekordu ze środków MEiN, umowa nr SONP/SP/546092/2022 w ramach programu "Społeczna odpowiedzialność nauki" - moduł: Popularyzacja nauki i promocja sportu (2022-2023).