3,846
Views
26
CrossRef citations to date
0
Altmetric
Research Article

From blood to brain: blood cell-based biomimetic drug delivery systems

ORCID Icon, , , , , & show all
Pages 1214-1225 | Received 26 Apr 2021, Accepted 25 May 2021, Published online: 18 Jun 2021

References

  • Abraham S, Soundararajan CC, Vivekanandhan S, Behari M. (2005). Erythrocyte antioxidant enzymes in Parkinson's disease. Indian J Med Res 121:111–5.
  • Anoop V, Cutinho LI, Mourya P, et al. (2020). Approaches for encephalic drug delivery using nanomaterials: the current status. Brain Res Bull 155:184–90.
  • Arvanitis CD, Ferraro GB, Jain RK. (2020). The blood–brain barrier and blood–tumour barrier in brain tumours and metastases. Nat Rev Cancer 20:26–41.
  • Banerjee M, Whiteheart SW. (2017). The ins and outs of endocytic trafficking in platelet functions. Curr Opin Hematol 24:467–74.
  • Barbero F, Russo L, Vitali M, et al. (2017). Formation of the protein corona: the interface between nanoparticles and the immune system. Semin Immunol 34:52–60.
  • Barnholtz-Sloan JS, Ostrom QT, Cote D. (2018). Epidemiology of brain tumors. Neurol Clin 36:395–419.
  • Becher B, Spath S, Goverman J. (2017). Cytokine networks in neuroinflammation. Nat Rev Immunol 17:49–59.
  • Bertrand N, Grenier P, Mahmoudi M, et al. (2017). Mechanistic understanding of in vivo protein corona formation on polymeric nanoparticles and impact on pharmacokinetics. Nat Commun 8:777.
  • Bhateria M, Rachumallu R, Singh R, Bhatta RS. (2014). Erythrocytes-based synthetic delivery systems: transition from conventional to novel engineering strategies. Expert Opin Drug Deliv 11:1219–36.
  • Bloem BR, Okun MS, Klein C. (2021). Parkinson's disease. Lancet;
  • Brailoiu E, Barlow CL, Ramirez SH, et al. (2018). Effects of platelet-activating factor on brain microvascular endothelial cells. Neuroscience 377:105–13.
  • Broen MP, Narayen NE, Kuijf ML, et al. (2016). Prevalence of anxiety in Parkinson's disease: a systematic review and meta-analysis. Mov Disord 31:1125–33.
  • Canepa E, Fossati S. (2020). Impact of tau on neurovascular pathology in Alzheimer's disease. Front Neurol 11:573324.
  • Castro F, Martins C, Silveira MJ, et al. (2021). Advances on erythrocyte-mimicking nanovehicles to overcome barriers in biological microenvironments. Adv Drug Deliv Rev 170:312–39.
  • Catanese L, Tarsia J, Fisher M. (2017). Acute ischemic stroke therapy overview. Circ Res 120:541–58.
  • Chai Z, Hu X, Wei X, et al. (2017). A facile approach to functionalizing cell membrane-coated nanoparticles with neurotoxin-derived peptide for brain-targeted drug delivery. J Control Release 264:102–11.
  • Chai Z, Ran D, Lu L, et al. (2019). Ligand-modified cell membrane enables the targeted delivery of drug nanocrystals to glioma. ACS Nano 13:5591–601.
  • Chen YX, Wei CX, Lyu YQ, et al. (2020). Biomimetic drug-delivery systems for the management of brain diseases. Biomater Sci 8:1073–88.
  • Chinen AB, Guan CM, Ko CH, Mirkin CA. (2017). The impact of protein corona formation on the macrophage cellular uptake and biodistribution of spherical nucleic acids. Small 13:1603847.
  • Choi MR, Bardhan R, Stanton-Maxey KJ, et al. (2012). Delivery of nanoparticles to brain metastases of breast cancer using a cellular Trojan horse. Cancer Nanotechnol 3:47–54.
  • Chouchani ET, Pell VR, Gaude E, et al. (2014). Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 515:431–5.
  • Chu AL, Hickman M, Steel N, et al. (2021). Inflammation and depression: a public health perspective. Brain Behav Immun;
  • D'amico RS, Aghi MK, Vogelbaum MA, Bruce JN. (2021). Convection-enhanced drug delivery for glioblastoma: a review. J Neurooncol 151:415–27.
  • De Lange ECM, Van Den Brink W, Yamamoto Y, et al. (2017). Novel CNS drug discovery and development approach: model-based integration to predict neuro-pharmacokinetics and pharmacodynamics. Expert Opin Drug Discov 12:1207–18.
  • Dong X, Gao J, Zhang CY, et al. (2019). Neutrophil membrane-derived nanovesicles alleviate inflammation to protect mouse brain injury from ischemic stroke. ACS Nano 13:1272–83.
  • D'Souza A, Dave KM, Stetler RA, Manickam DS. (2021). Targeting the blood–brain barrier for the delivery of stroke therapies. Adv Drug Deliv Rev 171:332–51.
  • Fang RH, Kroll AV, Gao W, Zhang L. (2018). Cell membrane coating nanotechnology. Adv Mater 30:e1706759.
  • Feng L, Dou C, Xia Y, et al. (2021). Neutrophil-like cell-membrane-coated nanozyme therapy for ischemic brain damage and long-term neurological functional recovery. ACS Nano 15:2263–80.
  • Ferraris C, Cavalli R, Panciani PP, Battaglia L. (2020). Overcoming the blood–brain barrier: successes and challenges in developing nanoparticle-mediated drug delivery systems for the treatment of brain tumours. Int J Nanomedicine 15:2999–3022.
  • Fromen CA, Kelley WJ, Fish MB, et al. (2017). Neutrophil-particle interactions in blood circulation drive particle clearance and alter neutrophil responses in acute inflammation. ACS Nano 11:10797–807.
  • Gangoso E, Southgate B, Bradley L, et al. (2021). Glioblastomas acquire myeloid-affiliated transcriptional programs via epigenetic immunoediting to elicit immune evasion. Cell 184:2454–2470.e26.
  • Gao H. (2016). Progress and perspectives on targeting nanoparticles for brain drug delivery. Acta Pharm Sin B 6:268–86.
  • Gao H. (2017). Perspectives on dual targeting delivery systems for brain tumors. J Neuroimmune Pharmacol 12:6–16.
  • Gao W, Hu CM, Fang RH, et al. (2013). Surface functionalization of gold nanoparticles with red blood cell membranes. Adv Mater 25:3549–53.
  • Gao X, Li S, Ding F, et al. (2021). A virus-mimicking nucleic acid nanogel reprograms microglia and macrophages for glioblastoma therapy. Adv Mater 33:e2006116.
  • Gao C, Wang H, Wang T, et al. (2020). Platelet regulates neuroinflammation and restores blood–brain barrier integrity in a mouse model of traumatic brain injury. J Neurochem 154:190–204.
  • Gribkoff VK, Kaczmarek LK. (2017). The need for new approaches in CNS drug discovery: why drugs have failed, and what can be done to improve outcomes. Neuropharmacology 120:11–9.
  • Hamidi M, Tajerzadeh H. (2003). Carrier erythrocytes: an overview. Drug Deliv 10:9–20.
  • Haney MJ, Klyachko NL, Zhao Y, et al. (2015). Exosomes as drug delivery vehicles for Parkinson's disease therapy. J Control Release 207:18–30.
  • Haumann R, Videira JC, Kaspers GJL, et al. (2020). Overview of current drug delivery methods across the blood–brain barrier for the treatment of primary brain tumors. CNS Drugs 34:1121–31.
  • Hou J, Yang X, Li S, et al. (2019). Accessing neuroinflammation sites: monocyte/neutrophil-mediated drug delivery for cerebral ischemia. Sci Adv 5:eaau8301.
  • Hu Q, Sun W, Qian C, et al. (2015). Anticancer platelet-mimicking nanovehicles. Adv Mater 27:7043–50.
  • Huang Y, Gao X, Chen J. (2018). Leukocyte-derived biomimetic nanoparticulate drug delivery systems for cancer therapy. Acta Pharm Sin B 8:4–13.
  • Hurford R, Wolters FJ, Li L, et al. (2020). Prevalence, predictors, and prognosis of symptomatic intracranial stenosis in patients with transient ischaemic attack or minor stroke: a population-based cohort study. Lancet Neurol 19:413–21.
  • Induruwa I, Moroi M, Bonna A, et al. (2018). Platelet collagen receptor glycoprotein VI-dimer recognizes fibrinogen and fibrin through their D-domains, contributing to platelet adhesion and activation during thrombus formation. J Thromb Haemost 16:389–404.
  • Jia G, Han Y, An Y, et al. (2018). NRP-1 targeted and cargo-loaded exosomes facilitate simultaneous imaging and therapy of glioma in vitro and in vivo. Biomaterials 178:302–16.
  • Kalia LV, Lang AE. (2015). Parkinson's disease. Lancet 386:896–912.
  • Kalluri R, Lebleu VS. (2020). The biology, function, and biomedical applications of exosomes. Science 367:eaau6977.
  • Kameritsch P, Renkawitz J. (2020). Principles of leukocyte migration strategies. Trends Cell Biol 30:818–32.
  • Khandelwal P, Yavagal DR, Sacco RL. (2016). Acute ischemic stroke intervention. J Am Coll Cardiol 67:2631–44.
  • Klyachko NL, Polak R, Haney MJ, et al. (2017). Macrophages with cellular backpacks for targeted drug delivery to the brain. Biomaterials 140:79–87.
  • Koupenova M, Clancy L, Corkrey HA, Freedman JE. (2018). Circulating platelets as mediators of immunity, inflammation, and thrombosis. Circ Res 122:337–51.
  • Koupenova M, Kehrel BE, Corkrey HA, Freedman JE. (2017). Thrombosis and platelets: an update. Eur Heart J 38:785–91.
  • Kroll AV, Fang RH, Zhang L. (2017). Biointerfacing and applications of cell membrane-coated nanoparticles. Bioconjug Chem 28:23–32.
  • Lapchak PA. (2010). A critical assessment of edaravone acute ischemic stroke efficacy trials: is edaravone an effective neuroprotective therapy? Expert Opin Pharmacother 11:1753–63.
  • Li M, Li J, Chen J, et al. (2020b). Platelet membrane biomimetic magnetic nanocarriers for targeted delivery and in situ generation of nitric oxide in early ischemic stroke. ACS Nano 14:2024–35.
  • Li M, Liu Y, Chen J, et al. (2018). Platelet bio-nanobubbles as microvascular recanalization nanoformulation for acute ischemic stroke lesion theranostics. Theranostics 8:4870–83.
  • Liu Y, Wang M, Wang D, et al. (2021). Elevated post-ischemic tissue injury and leukocyte–endothelial adhesive interactions in mice with global deficiency in caveolin-2: role of PAI-1. Am J Physiol Heart Circ Physiol;
  • Li F, Zhao L, Shi Y, Liang J. (2020a). Edaravone-loaded macrophage-derived exosomes enhance neuroprotection in the rat permanent middle cerebral artery occlusion model of stroke. Mol Pharm 17:3192–201.
  • Lu Y, He HJ, Zhou J, et al. (2013). Hyperphosphorylation results in tau dysfunction in DNA folding and protection. J Alzheimers Dis 37:551–63.
  • Lu Y, Hu Q, Jiang C, Gu Z. (2019). Platelet for drug delivery. Curr Opin Biotechnol 58:81–91.
  • Luk BT, Zhang L. (2015). Cell membrane-camouflaged nanoparticles for drug delivery. J Control Release 220:600–7.
  • Lv Y, Ma X, Du Y, Feng J. (2021). Understanding patterns of brain metastasis in triple-negative breast cancer and exploring potential therapeutic targets. Onco Targets Ther 14:589–607.
  • Mailles A, Stahl JP, Bloch KC. (2017). Update and new insights in encephalitis. Clin Microbiol Infect 23:607–13.
  • Miller G. (2010). Is pharma running out of brainy ideas? Science 329:502–4.
  • Morad G, Carman CV, Hagedorn EJ, et al. (2019). Tumor-derived extracellular vesicles breach the intact blood–brain barrier via transcytosis. ACS Nano 13:13853–65.
  • Okuda M, Hijikuro I, Fujita Y, et al. (2016). Design and synthesis of curcumin derivatives as tau and amyloid β dual aggregation inhibitors. Bioorg Med Chem Lett 26:5024–8.
  • Ostrom QT, Gittleman H, Xu J, et al. (2016). CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2009–2013. Neuro Oncol 18:v1–v75.
  • Pang L, Zhu Y, Qin J, et al. (2018). Primary M1 macrophages as multifunctional carrier combined with PLGA nanoparticle delivering anticancer drug for efficient glioma therapy. Drug Deliv 25:1922–31.
  • Parodi A, Quattrocchi N, Van De Ven AL, et al. (2013). Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat Nanotechnol 8:61–8.
  • Patel RaG, McMullen PW. (2017). Neuroprotection in the treatment of acute ischemic stroke. Prog Cardiovasc Dis 59:542–8.
  • Pegtel DM, Gould SJ. (2019). Exosomes. Annu Rev Biochem 88:487–514.
  • Piper K, Depledge L, Karsy M, Cobbs C. (2021). Glioma stem cells as immunotherapeutic targets: advancements and challenges. Front Oncol 11:615704.
  • Qin J, Yang X, Zhang RX, et al. (2015). Monocyte mediated brain targeting delivery of macromolecular drug for the therapy of depression. Nanomedicine 11:391–400.
  • Reddy S, Tatiaparti K, Sau S, Iyer AK. (2021). Recent advances in nano delivery systems for blood–brain barrier (BBB) penetration and targeting of brain tumors. Drug Discov Today;
  • Rochette F, Engelen M, Vanden Bossche H. (2003). Antifungal agents of use in animal health-practical applications. J Vet Pharmacol Ther 26:31–53.
  • Ruan S, Zhou Y, Jiang X, Gao H. (2021). Rethinking CRITID procedure of brain targeting drug delivery: circulation, blood brain barrier recognition, intracellular transport, diseased cell targeting, internalization, and drug release. Adv Sci (Weinh) 8:2004025.
  • Russell LM, Hultz M, Searson PC. (2018). Leakage kinetics of the liposomal chemotherapeutic agent doxil: the role of dissolution, protonation, and passive transport, and implications for mechanism of action. J Control Release 269:171–6.
  • Scheltens P, De Strooper B, Kivipelto M, et al. (2021). Alzheimer's disease. Lancet;
  • Shi Q, Montgomery RR. (2010). Platelets as delivery systems for disease treatments. Adv Drug Deliv Rev 62:1196–203.
  • Shi J, Yu W, Xu L, et al. (2020). Bioinspired nanosponge for salvaging ischemic stroke via free radical scavenging and self-adapted oxygen regulating. Nano Lett 20:780–9.
  • Shi HS, Zhu WL, Liu JF, et al. (2012). PI3K/Akt signaling pathway in the basolateral amygdala mediates the rapid antidepressant-like effects of trefoil factor 3. Neuropsychopharmacology 37:2671–83.
  • Song G, Zhao M, Chen H, et al. (2021). The role of nanomaterials in stroke treatment: targeting oxidative stress. Oxid Med Cell Longev 2021:8857486.
  • Spite M, Norling LV, Summers L, et al. (2009). Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 461:1287–91.
  • Stanimirovic DB, Bani-Yaghoub M, Perkins M, Haqqani AS. (2015). Blood–brain barrier models: in vitro to in vivo translation in preclinical development of CNS-targeting biotherapeutics. Expert Opin Drug Discov 10:141–55.
  • Sun Y, Su J, Liu G, et al. (2017). Advances of blood cell-based drug delivery systems. Eur J Pharm Sci 96:115–28.
  • Usman WM, Pham TC, Kwok YY, et al. (2018). Efficient RNA drug delivery using red blood cell extracellular vesicles. Nat Commun 9:2359.
  • Vacha R, Martinez-Veracoechea FJ, Frenkel D. (2011). Receptor-mediated endocytosis of nanoparticles of various shapes. Nano Lett 11:5391–5.
  • Van Tellingen O, Yetkin-Arik B, De Gooijer MC, et al. (2015). Overcoming the blood–brain tumor barrier for effective glioblastoma treatment. Drug Resist Updat 19:1–12.
  • Vissers C, Ming GL, Song H. (2019). Nanoparticle technology and stem cell therapy team up against neurodegenerative disorders. Adv Drug Deliv Rev 148:239–51.
  • Vuillemenot BR, Korte S, Wright TL, et al. (2016). Safety evaluation of CNS administered biologics-study design, data interpretation, and translation to the clinic. Toxicol Sci 152:3–9.
  • Wang Q, Cheng H, Peng H, et al. (2015). Non-genetic engineering of cells for drug delivery and cell-based therapy. Adv Drug Deliv Rev 91:125–40.
  • Wang C, Li K, Li T, et al. (2018). Monocyte-mediated chemotherapy drug delivery in glioblastoma. Nanomedicine (Lond) 13:157–78.
  • Wang H, Sui H, Zheng Y, et al. (2019). Curcumin-primed exosomes potently ameliorate cognitive function in AD mice by inhibiting hyperphosphorylation of the Tau protein through the AKT/GSK-3β pathway. Nanoscale 11:7481–96.
  • Wang J, Tang W, Yang M, et al. (2021). Inflammatory tumor microenvironment responsive neutrophil exosomes-based drug delivery system for targeted glioma therapy. Biomaterials 273:120784.
  • Watanabe T, Tahara M, Todo S. (2008). The novel antioxidant edaravone: from bench to bedside. Cardiovasc Ther 26:101–14.
  • Wei X, Ying M, Dehaini D, et al. (2018). Nanoparticle functionalization with platelet membrane enables multifactored biological targeting and detection of atherosclerosis. ACS Nano 12:109–16.
  • Wei X, Zhan C, Shen Q, et al. (2015). A D-peptide ligand of nicotine acetylcholine receptors for brain-targeted drug delivery. Angew Chem Int Ed Engl 54:3023–7.
  • Wu M, Zhang H, Tie C, et al. (2018). MR imaging tracking of inflammation-activatable engineered neutrophils for targeted therapy of surgically treated glioma. Nat Commun 9:4777.
  • Xia Q, Zhang Y, Li Z, et al. (2019). Red blood cell membrane-camouflaged nanoparticles: a novel drug delivery system for antitumor application. Acta Pharm Sin B 9:675–89.
  • Xie J, Shen Z, Anraku Y, et al. (2019). Nanomaterial-based blood–brain-barrier (BBB) crossing strategies. Biomaterials 224:119491.
  • Xu J, Wang X, Yin H, et al. (2019). Sequentially site-specific delivery of thrombolytics and neuroprotectant for enhanced treatment of ischemic stroke. ACS Nano 13:8577–88.
  • Xue J, Zhao Z, Zhang L, et al. (2017). Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence. Nat Nanotechnol 12:692–700.
  • Yamamoto Y, Valitalo PA, Wong YC, et al. (2018). Prediction of human CNS pharmacokinetics using a physiologically-based pharmacokinetic modeling approach. Eur J Pharm Sci 112:168–79.
  • Yang Q, Guo N, Zhou Y, et al. (2020). The role of tumor-associated macrophages (TAMs) in tumor progression and relevant advance in targeted therapy. Acta Pharm Sin B 10:2156–70.
  • Ye ZP, Ai XL, Faramand AM, Fang F. (2018). Macrophages as nanocarriers for drug delivery: novel therapeutics for central nervous system diseases. J Nanosci Nanotechnol 18:471–85.
  • Yoo JW, Irvine DJ, Discher DE, Mitragotri S. (2011). Bio-inspired, bioengineered and biomimetic drug delivery carriers. Nat Rev Drug Discov 10:521–35.
  • Yuan D, Zhao Y, Banks WA, et al. (2017). Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials 142:1–12.
  • Zhang C, Ling CL, Pang L, et al. (2017). Direct macromolecular drug delivery to cerebral ischemia area using neutrophil-mediated nanoparticles. Theranostics 7:3260–75.
  • Zhang W, Wang M, Tang W, et al. (2018). Nanoparticle-laden macrophages for tumor-tropic drug delivery. Adv Mater 30:e1805557.
  • Zhao L, Xu YH, Akasaka T, et al. (2014). Polyglycerol-coated nanodiamond as a macrophage-evading platform for selective drug delivery in cancer cells. Biomaterials 35:5393–406.
  • Zhou L, Li F, Xu HB, et al. (2010). Treatment of cerebral ischemia by disrupting ischemia-induced interaction of nNOS with PSD-95. Nat Med 16:1439–43.
  • Zimmer AS, Van Swearingen AED, Anders CK. (2020). HER2-positive breast cancer brain metastasis: a new and exciting landscape. Cancer Rep (Hoboken) e1274.