Cited by 116RNA Interference and Gene DeliveryNanoparticle-Based Drug DeliveryBarrier Structure and Function Studies

Dual functionalized liposome-mediated gene delivery across triple co-culture blood brain barrier model and specific in vivo neuronal transfection

Open access
dos Santos Rodrigues, Bruna, Oue, Hiroshi, Banerjee, Amrita, Kanekiyo, Takahisa, Singh, Jagdish·2018·Journal of Controlled Release

Abstract

Gene therapy has become a promising approach for neurodegenerative disease treatment, however there is an urgent need to develop an efficient gene carrier to transport gene across the blood brain barrier (BBB). In this study, we strategically designed dual functionalized liposomes for efficient neuronal transfection by combining transferrin (Tf) receptor targeting and enhanced cell penetration utilizing penetratin (Pen). A triple cell co-culture model of BBB confirmed the ability of the liposomes to cross the barrier layer and transfect primary neuronal cells. In vivo quantification of PenTf-liposomes demonstrated expressive accumulation in the brain (12%), without any detectable cellular damage or morphological change. The efficacy of these nanoparticles containing plasmid β-galactosidase in modulating transfection was assessed by β-galactosidase expression in vivo. As a consequence of accumulation in the brain, PenTf-liposomes significantly induced gene expression in mice. Immunofluorescence studies of brain sections of mice after tail vein injection of liposomes encapsulating pDNA encoding GFP (pGFP) illustrate the superior ability of dual-functionalized liposomes to accumulate in the brain and transfect neurons. Taken together, the multifunctional liposomes provide an excellent gene delivery platform for neurodegenerative diseases.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.jconrel.2018.07.043

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • CBP/p300 transcriptional co-activators are a conserved mechanism for responding to mitochondrial stress.

    “The CBP/p300 transcriptional co-activators are a conserved mechanism for responding to mitochondrial stress”

    From Rlip76: An Unexplored Player in Neurodegeneration and Alzheimer’s Disease? (2022) · cites this paper as [117]

    The Introduction and Conclusions describe liposomes designed to cross the blood–brain barrier and deliver genes to neurons. Searches for CBP/p300 and for a conserved mitochondrial-stress response found no passage addressing either point in our copy. (LLM, conf=0.78)

    Experimental — accuracy not yet measured
  • Loss of function of CBP/p300 is associated with familial AD and neuronal apoptosis.

    “and the loss of function of CBP/p300 is associated with familial AD and neuronal apoptosis [117,118,119,120,121].”

    From Rlip76: An Unexplored Player in Neurodegeneration and Alzheimer’s Disease? (2022) · cites this paper as [117]

    The Introduction discusses Alzheimer’s disease as a potential target for brain-directed gene delivery, but does not discuss CBP/p300 or familial AD. The Conclusions address neuronal transfection by liposomes, not neuronal apoptosis. Searches for CBP/p300 loss of function and related terms found no passage supporting the claimed association; the indexed passages provide no page numbers. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 86

  1. [3]Jeffrey P, Summer S, Neurobiology of Disease Assessment of the blood - brain barrier in CNS drug discovery, 37 (2010) 33– 37. doi: 10.1016/j.nbd.2009.07.033. 19664709 · DOI
  2. [6]Pardo J, Morel GR, Astiz M, Schwerdt JI, León ML, Rodríguez SS, Hereñú CB, Goya RG, Gene Therapy and Cell Reprogramming for the Aging Brain: Achieve- ments and Promise, (2014) 24– 34. 24450294
  3. [7]Yin H, Kanasty RL, Eltoukhy AA, Vegas AJ, Dorkin JR, Anderson DG, Non- viral vectors for gene-based therapy, Nat Rev Genet. 15 (2014) 541– 555. doi: 10.1038/nrg3763. 25022906 · DOI · Paper page
  4. [8]Liu Y, An S, Li J, Kuang Y, He X, Guo Y, Ma H, Biomaterials Brain-targeted co-delivery of therapeutic gene and peptide by multifunctional nanoparticles in Alzheimer ‘ s disease mice, 80 (2016) 33– 45. doi: 10.1016/j.biomaterials.2015.11.060. 26706474 · DOI
  5. [9]Zheng X, Zhang C, Guo Q, Wan X, Shao X, Liu Q, Zhang Q, Dual-functional nanoparticles for precise drug delivery to Alzheimer’s disease lesions: Targeting mechanisms, pharmacodynamics and safety, Int. J. Pharm. 525 (2017) 237– 248. doi: 10.1016/j.ijpharm.2017.04.033. 28432017 · DOI
  6. [10]Ordóñez-Gutiérrez L, Posado-Fernández A, Ahmadvand D, Lettiero B, Wu L, Antón M, Flores O, Moghimi SM, Wandosell F, ImmunoPEGliposome-mediated reduction of blood and brain amyloid levels in a mouse model of Alzheimer’s disease is restricted to aged animals, Biomaterials. 112 (2016). doi: 10.1016/j.biomaterials.2016.07.027. 27760398 · DOI
  7. [11]Gregori M, Taylor M, Salvati E, Re F, Mancini S, Balducci C, Forloni G, Zambelli V, Sesana S, Michael M, Michail C, Tinker-Mill C, Kolosov O, Scherer M, Harris S, Fullwood NJ, Masserini M, Allsop D, Retro-inverso peptide inhibitor nanoparticles as potent inhibitors of aggregation of the Alzheimer’s Αβ peptide, Nanomedicine Nanotechnology, Biol. Med. (2016) 1– 10. doi: 10.1016/j.nano.2016.10.006. 27769888 · DOI
  8. [12]Sánchez-López E, Ettcheto M, Egea MA, Espina M, Calpena AC, Folch J, Camins A, García ML, New Potential Strategies for Alzheimer’s Disease Prevention: Pegylated Biodegradable Dexibuprofen Nanospheres Administration to APPswe/PSldE9, Nanomedicine Nanotechnology, Biol. Med. (2016). doi: 10.1016/j.nano.2016.12.003. 27986603 · DOI
  9. [13]Tapeinos C, Battaglini M, Ciofani G, Advances in the design of solid lipid nanoparticles and nanostructured lipid carriers for targeting brain diseases, J. Control. Release. 264 (2017) 306– 332. doi: 10.1016/j.jconrel.2017.08.033. 28844756 PMC6701993 · DOI
  10. [14]Obata Y, Saito S, Takeda N, Takeoka S, Plasmid DNA-encapsulating liposomes: Effect of a spacer between the cationic head group and hydrophobic moieties of the lipids on gene expression efficiency, Biochim. Biophys. Acta - Biomembr. 1788 (2009) 1148– 1158. doi: 10.1016/j.bbamem.2009.02.014. 19249283 · DOI
  11. [15]Yang Y, Yang Y, Xie X, Cai X, Zhang H, Gong W, Wang Z, Mei X, Biomaterials PEGylated liposomes with NGR ligand and heat-activable cell- penetrating peptide e doxorubicin conjugate for tumor-specific therapy, Biomaterials. 35 (2014) 4368– 4381. doi: 10.1016/j.biomaterials.2014.01.076. 24565519 · DOI
  12. [16]Vieira DB, Gamarra LF, Getting into the brain: Liposome-based strategies for effective drug delivery across the blood-brain barrier, Int. J. Nanomedicine. 11 (2016) 5381– 5414. doi: 10.2147/UN.S117210. PMC5077137 27799765 · DOI
  13. [17]Paterson J, Webster CI, Exploiting transferrin receptor for delivering drugs across the blood-brain barrier, Drug Discov. Today Technol. 20 (2016) 49– 52. doi: 10.1016/j.ddtec.2016.07.009. 27986223 · DOI · Paper page
  14. [18]Agrawal M, Ajazuddin, Tripathi DK, Saraf S, Saraf S, Antimisiaris SG, Mourtas S, Hammarlund-Udenaes M, Alexander A, Recent advancements in liposomes targeting strategies to cross blood-brain barrier (BBB) for the treatment of Alzheimer’s disease, J. Control. Release. 260 (2017) 61– 77. doi: 10.1016/j.jconrel.2017.05.019. 28549949 · DOI · Paper page
  15. [19]Gatter KC, Brown G, Trowbridge IS, Woolston RE, Mason DY, Transferrin receptors in human tissues: their distribution and possible clinical relevance., J. Clin. Pathol. 36 (1983) 539– 545. doi: 10.1136/jcp.36.5.539. 6302135 PMC498283 · DOI
  16. [20]Hersom M, Helms HC, Pretzer N, Goldeman C, Jensen AI, Severin G, Nielsen MS, Holm R, Brodin B, Transferrin receptor expression and role in transendothelial transport of transferrin in cultured brain endothelial monolayers, (2016). doi: 10.1016/j.men.2016.08.009. 27567687 · DOI
  17. [21]Jefferies WA, Brandon MR, V Hunt S, Williams AF, Gatter KC, Mason DY, Transferrin receptor on endothelium of brain capillaries., Nature. 312 (n.d.) 162– 3. http://www.ncbi.nlm.nih.gov/pubmed/6095085 (accessed December 6, 2017). 6095085
  18. [22]Johnsen KB, Moos T, Revisiting nanoparticle technology for blood-brain barrier transport: Unfolding at the endothelial gate improves the fate of transferrin receptor- targeted liposomes, J. Control. Release. 222 (2016) 32– 46. doi: 10.1016/j.jconrel.2015.11.032. 26658072 · DOI
  19. [23]Xiao G, Gan L-S, Receptor-mediated endocytosis and brain delivery of therapeutic biologies., Int. J. Cell Biol 2013 (2013) 703545. doi: 10.1155/2013/703545. 23840214 PMC3693099 · DOI
  20. [24]Srinivasarao M, Low PS, Ligand-Targeted Drug Delivery, Chem. Rev. 117 (2017) 12133– 12164. doi: 10.1021/acs.chemrev.7b00013. 28898067 · DOI
  21. [25]Zhang D, Wang J, Xu D, Cell-penetrating peptides as noninvasive transmembrane vectors for the development of novel multifunctional drug-delivery systems, J. Control. Release. 229 (2016) 130– 139. doi: 10.1016/j.jconrel.2016.03.020. 26993425 · DOI
  22. [26]Bashyal S, Noh G, Keum T, Choi YW, Lee S, Cell penetrating peptides as an innovative approach for drug delivery; then, present and the future, J. Pharm. Investig. 46 (2016) 205– 220. doi: 10.1007/s40005-016-0253-0. · DOI
  23. [27]Brugnano J, Ward BC, Panitch A, Cell penetrating peptides can exert biological activity: A review, Biomol. Concepts. 1 (2010) 109– 116. doi: 10.1515/bmc.2010.016. 25961990 · DOI
  24. [28]Yang Z, Li J, Wang Z, Dong D, Qi X, Biomaterials Tumor-targeting dual peptides- modi fi ed cationic liposomes for delivery of siRNA and docetaxel to gliomas, Biomaterials. 35 (2014) 5226– 5239. doi: 10.1016/j.biomaterials.2014.03.017. 24695093 · DOI
  25. [29]Sharma G, Modgil A, Layek B, Arora K, Sun C, Law B, Singh J, Cell penetrating peptide tethered bi-ligand liposomes for delivery to brain in vivo: Biodistribution and transfection, J. Control. Release. 167 (2013) 1– 10. doi: 10.1016/j.jconrel.2013.01.016. 23352910 · DOI
  26. [30]Pankevich DE, Altevogt BM, Dunlop J, Gage FH, Hyman SE, Improving and accelerating drug development for nervous system disorders, Neuron. 84 (2014) 546– 553. doi: 10.1016/j.neuron.2014.10.007. 25442933 PMC4254615 · DOI
  27. [31]Cifani N, Chronopoulou L, Pompili B, Di A, @bullet M, Bordi F, Sennato S, Enea @bullet, Di G, @bulle D, Palocci C, Ascenzioni F, Improved stability and efficacy of chitosan/pDNA complexes for gene delivery, (2014). doi: 10.1007/sl0529-014-1727-7. 25388452 · DOI
  28. [32]Nimesh S, Thibault MM, Lavertu M, Buschmann MD, Enhanced Gene Delivery Mediated by Low Molecular Weight Chitosan/DNA Complexes: Effect of pH and Serum, (2010). doi: 10.1007/s12033-010-9286-1. PMC2929434 20454872 · DOI
  29. [33]Sumners C, Fregly MJ, Modulation of angiotensin II binding sites in neuronal cultures by mineralocorticoids, Am. J. Physiol. 256 (1989) C121– C129. 2912130
  30. [34]Sumners C, Tang WEI, Raizada MK, Angiotensin II receptor subtypes are coupled with distinct signal-transduction mechanisms in neurons and astrocytes from rat brain, Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 7567– 7571. 1881896 PMC52342
  31. [35]Nakagawa S, Deli MA, Kawaguchi H, Shimizudani T, Shimono T, Kittel Á, Tanaka K, Niwa M, A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes, Neurochem. Int. 54 (2009) 253– 263. doi: 10.1016/j.neuint.2008.12.002. 19111869 · DOI · Paper page
  32. [36]Helms HC, Abbott NJ, Burek M, Cecchelli R, Couraud P-O, Deli MA, Förster C, Galla HJ, Romero IA, Shusta EV, Stebbins MJ, Vandenhaute E, Weksler B, Brodin B, In vitro models of the blood-brain barrier: An overview of commonly used brain endothelial cell culture models and guidelines for their use, J. Cereb. Blood FlowMetab. 36 (2016) 862– 890. doi: 10.1177/0271678X16630991. PMC4853841 26868179 · DOI · Paper page
  33. [37]Sharma G, Modgil A, Sun C, Singh J, Grafting of cell-penetrating peptide to receptor-targeted liposomes improves their transfection efficiency and transport across blood-brain barrier model., J. Pharm. Sci. 101 (2012) 2468– 78. doi: 10.1002/jps.23152. 22517732 · DOI
  34. [38]Xue Q, Liu Y, Qi H, Ma Q, Xu L, Chen W, Chen G, Xu X, A novel brain neurovascular unit model with neurons, astrocytes and microvascular endothelial cells of rat, Int. J. Biol. Sci. 9 (2013) 174– 189. doi: 10.7150/ijbs.5115. 23412420 PMC3572400 · DOI
  35. [39]Ashok B, Arleth L, Hjelm RP, Rubinstein I, Önyüksel H, In vitro characterization of PEGylated phospholipid micelles for improved drug solubilization: Effects of PEG chain length and PC incorporation, J. Pharm. Sci. (2004). doi: 10.1002/jps.20150. 15349957 · DOI
  36. [40]Bana L, Minniti S, Salvati E, Sesana S, Zambelli V, Cagnotto A, Orlando A, Cazzaniga E, Zwart R, Scheper W, Masserini M, Re F, Liposomes bi-functionalized with phosphatidic acid and an ApoE-derived peptide affect A?? aggregation features and cross the blood-brain-barrier: Implications for therapy of Alzheimer disease, Nanomedicine Nanotechnology, Biol. Med. 10 (2014) 1583– 1590. doi: 10.1016/j.nano.2013.12.001. 24333591 · DOI
  37. [41]Balducci C, Mancini S, Minniti S, La Vitola P, Zotti M, Sancini G, Mauri M, Cagnotto A, Colombo L, Fiordaliso F, Grigoli E, Salmona M, Snellman A, Haaparanta-Solin M, Forloni G, Masserini M, Re F, Multifunctional Liposomes Reduce Brain -Amyloid Burden and Ameliorate Memory Impairment in Alzheimer’s Disease Mouse Models, J. Neurosci. 34 (2014) 14022– 14031. doi: 10.1523/JNEUROSCI.0284-14.2014. 25319699 PMC4198543 · DOI · Paper page
  38. [42]Li X, Wang L, Fan Y, Feng Q, Cui FZ, Biocompatibility and toxicity of nanoparticles and nanotubes, J. Nanomater. 2012 (2012). doi: 10.1155/2012/548389. · DOI
  39. [43]Hung S-Y, Fu W-M, Drug candidates in clinical trials for Alzheimer’s disease, J. Biomed. Sci. 24 (2017) 47. doi: 10.1186/sl2929-017-0355-7. 28720101 PMC5516350 · DOI
  40. [45]Sercombe L, Veerati T, Moheimani F, Wu SY, Sood AK, Hua S, Advances and challenges of liposome assisted drug delivery, Front. Pharmacol. 6 (2015) 1– 13. doi: 10.3389/fphar.2015.00286. 26648870 PMC4664963 · DOI
  41. [46]Bulbake U, Doppalapudi S, Kommineni N, Khan W, Liposomal formulations in clinical use: An updated review, Pharmaceutics. 9 (2017) 1– 33. doi: 10.3390/pharmaceutics9020012. PMC5489929 28346375 · DOI
  42. [47]Van Rooy I, Mastrobattista E, Storm G, Hennink WE, Schiffelers RM, Comparison of five different targeting ligands to enhance accumulation of liposomes into the brain, J. Control. Release. 150 (2011) 30– 36. doi: 10.1016/j.jconrel.2010.11.014. 21087646 · DOI
  43. [48]Salmaso S, Caliceti P, Stealth Properties to Improve Therapeutic Efficacy of Drug Nanocarriers, J. Drug Deliv. 2013 (2013) 1– 19. doi: 10.1155/2013/374252. PMC3606770 23533769 · DOI
  44. [49]Lee HJ, Engelhardt B, Lesley J, Bickel U, Pardridge WM, Targeting rat anti-mouse transferrin receptor monoclonal antibodies through blood-brain barrier in mouse., J. Pharmacol. Exp. Ther. 292 (2000) 1048– 1052. 10688622
  45. [50]Stalmans S, Bracke N, Wynendaele E, Gevaert B, Peremans K, Burvenich C, Polis I, De Spiegeleer B, Cell-penetrating peptides selectively cross the blood-brain barrier in vivo, PLoS One. 10 (2015) 1– 22. doi: 10.1371/joumal.pone.0139652. PMC4605843 26465925 · DOI
  46. [51]Ramsey JD, Flynn NH, Cell-penetrating peptides transport therapeutics into cells, Pharmacol. Ther. 154 (2015) 78– 86. doi: 10.1016/j.pharmthera.2015.07.003. 26210404 · DOI
  47. [52]Kamei N, Morishita M, Eda Y, Ida N, Nishio R, Takayama K, Usefulness of cell- penetrating peptides to improve intestinal insulin absorption, J. Control. Release. 132 (2008) 21– 25. doi: 10.1016/j.jconrel.2008.08.001. 18727945 · DOI
  48. [53]Jain M, Chauhan SC, Singh AP, Venkatraman G, Colcher D, Batra SK, Penetratin improves tumor retention of single-chain antibodies: A novel step toward optimization of radioimmunotherapy of solid tumors, Cancer Res. 65 (2005) 7840– 7846. doi: 10.1158/0008-5472.CAN-05-0662. 16140953 · DOI
  49. [54]Mao S, Sun W, Kissel T, Chitosan-based formulations for delivery of DNA and siRNA, Adv. DrugDeliv. Rev. 62 (2010) 12– 27. doi: 10.1016/j.addr.2009.08.004. 19796660 · DOI
  50. [55]Mansouri S, Lavigne P, Corsi K, Benderdour M, Beaumont E, Fernandes JC, Chitosan-DNA nanoparticles as non-viral vectors in gene therapy: Strategies to improve transfection efficacy, Eur. J. Pharm. Biopharm. (2004). doi: 10.1016/S0939-6411(03)00155-3. 14729076 · DOI
  51. [56]Lavertu M, Méthot S, Tran-Khanh N, Buschmann MD, High efficiency gene transfer using chitosan/DNA nanoparticles with specific combinations of molecular weight and degree of deacetylation, Biomaterials. (2006). doi: 10.1016/j.biomaterials.2006.04.029. 16725196 · DOI
  52. [57]Lee S, Sato Y, Hyodo M, Harashima H, Topology of Surface Ligands on Liposomes: Characterization Based on the Terms, Incorporation Ratio, Surface Anchor Density, and Reaction Yield, 39 (2016) 1983– 1994. doi: 10.1248/bpb.bl6-00462. 27904040 · DOI
  53. [58]Marqués-Gallego P, De Kroon AIPM, Ligation strategies for targeting liposomal nanocarriers, Biomed Res. Int. 2014 (2014). doi: 10.1155/2014/129458. PMC4122157 25126543 · DOI
  54. [59]Nakamura K, Yamashita K, Itoh Y, Yoshino K, Nozawa S, Kasukawa H, Biochimica et Biophysica Acta Comparative studies of polyethylene glycol-modi fi ed liposomes prepared using different PEG-modi fi cation methods, BBA - Biomembr. 1818 (2012) 2801– 2807. doi: 10.1016/j.bbamem.2012.06.019. 22766474 · DOI
  55. [60]Nag OK, Awasthi V, Surface engineering of liposomes for stealth behavior, Pharmaceutics. (2013). doi: 10.3390/pharmaceutics5040542. PMC3873679 24300562 · DOI
  56. [61]Wu X, Gehring W, Cellular uptake of the Antennapedia homeodomain polypeptide by macropinocytosis, Biochem. Biophys. Res. Commun. 443 (2014) 1136– 1140. doi: 10.1016/j.bbrc.2013.12.062. 24361959 · DOI
  57. [62]Thevis M, Ogorzalek Loo RR, Loo JA, Mass spectrometric characterization of transferrins and their fragments derived by reduction of disulfide bonds, J. Am. Soc. Mass Spectrom. 14 (2003) 635– 647. doi: 10.1016/S1044-0305(03)00199-5. 12781465 · DOI
  58. [63]Aparicio-Blanco J, Martin-Sabroso C, Torres-Suárez A-I, In vitro screening of nanomedicines through the blood brain barrier: A critical review., Biomaterials. 103 (2016) 229– 55. doi: 10.1016/j.biomaterials.2016.06.051. 27392291 · DOI
  59. [64]Grabrucker AM, Ruozi B, Belletti D, Pederzoli F, Forni F, Vandelli MA, Tosi G, Grabrucker AM, Ruozi B, Belletti D, Pederzoli F, Forni F, Vandelli MA, Tosi G, Grabrucker AM, Ruozi B, Belletti D, Pederzoli F, Forni F, Vandelli MA, Tosi G, Nanoparticle transport across the blood brain barrier Nanoparticle transport across the blood brain barrier, 8370 (2016) 1– 18. doi: 10.1080/21688370.2016.1153568. · DOI · Paper page
  60. [65]Qi P, Cao M, Song L, Chen C, Liu M, Li N, Wu D, Peng J, Hu G, Zhao J, The biological activity of cationic liposomes in drug delivery and toxicity test in animal models, Environ. Toxicol. Pharmacol. 47 (2016) 159– 164. doi: 10.1016/j.etap.2016.09.015. 27694054 · DOI
  61. [66]Chou C-H, Sinden JD, Couraud P-O, Modo M, In Vitro Modeling of the Neurovascular Environment by Coculturing Adult Human Brain Endothelial Cells with Human Neural Stem Cells, PLoS One. 9 (2014) el06346. doi: 10.1371/journal.pone.0106346. PMC4154686 25187991 · DOI
  62. [67]Cecchelli R, Dehouck B, Descamps L, Fenart L, Buee-Scherrer V, Duhem C, Lundquist S, Rentfel M, Torpier G, Dehouck MP, In vitro model for evaluating drug transport across the blood-brain barrier, Adv. Drug Deliv. Rev 36 (1999) 165– 178. doi: 10.1016/S0169-409X(98)00083-0. 10837714 · DOI
  63. [68]Burkhart A, Skjørringe T, Johnsen KB, Siupka P, Thomsen LB, Nielsen MS, Thomsen LL, Moos T, Expression of Iron-Related Proteins at the Neurovascular Unit Supports Reduction and Reoxidation of Iron for Transport Through the Blood- Brain Barrier, Mol. Neurobiol. 53 (2016) 7237– 7253. doi: 10.1007/s12035-015-9582-7. 26687231 · DOI
  64. [69]Ponka P, Lok CN, The transferrin receptor: role in health and disease., Int. J. Biochem. Cell Biol 31 (1999) 1111– 37. http://www.ncbi.nlm.nih.gov/pubmed/10582342 (accessed October 25, 2015). 10582342
  65. [70]Vogel W, Bomford A, Young S, Williams R, Heterogeneous Distribution of Transferrin Receptors on Parenchymal and Nonparenchymal Liver Cells: Biochemical and Morphological Evidence, Blood. 69 (1987) 264– 270. http://www.bloodjournal.Org/content/bloodjournal/69/l/264.full.pdf (accessed April 4, 2018). 3539227
  66. [71]Uchida Y, Ohtsuki S, Katsukura Y, Ikeda C, Suzuki T, Kamiie J, Terasaki T, Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors, J. Neurochem. 117 (2011) 333– 345. doi: 10.1111/j.1471-4159.2011.07208.x. 21291474 · DOI · Paper page
  67. [72]Qian ZM, To Y, Tang PL, Feng YM, Transferrin receptors on the plasma membrane of cultured rat astrocytes., Exp.Brain Res. 129 (1999) 473– 476. 10591920
  68. [73]Fotticchia I, Guarnieri D, Fotticchia T, Falanga AP, Vecchione R, Giancola C, Netti PA, Energetics of ligand-receptor binding affinity on endothelial cells: An in vitro model, Colloids Surfaces B Biointerfaces. 144 (2016) 250– 256. doi: 10.1016/j.colsurfb.2016.04.018. 27100851 · DOI
  69. [74]Tarasoff-Conway JM, Carare RO, Osorio RS, Glodzik L, Butler T, Fieremans E, Axel L, Rusinek H, Nicholson C, Zlokovic BV, Frangione B, Blennow K, Ménard J, Zetterberg H, Wisniewski T, de Leon MJ, Clearance systems in the brain implications for Alzheimer disease, Nat. Rev. Neurol. 11 (2015) 457– 470. doi: 10.1038/nrneurol.2015.119. 26195256 PMC4694579 · DOI · Paper page
  70. [75]Bakker ENTP, Bacskai BJ, Arbel-Ornath M, Aldea R, Bedussi B, Morris AWJ, Weller RO, Carare RO, Lymphatic Clearance of the Brain: Perivascular, Paravascular and Significance for Neurodegenerative Diseases, Cell. Mol. Neurobiol. 36(2016) 181– 194. doi: 10.1007/s10571-015-0273-8. 26993512 PMC4844641 · DOI · Paper page
  71. [76]Zhang W, Peng F, Zhou T, Huang Y, Zhang L, Ye P, Lu M, Yang G, Gai Y, Yang T, Ma X, Xiang G, Targeted delivery of chemically modified anti-miR-221 to hepatocellular carcinoma with negatively charged liposomes, Int. J. Nanomedicine. 10 (2015) 4825– 4836. doi: 10.2147/UN.S79598. 26251599 PMC4524461 · DOI
  72. [77]Wang T, Yin X, Lu Y, Shan W, Xiong S, Formulation, antileukemia mechanism, pharmacokinetics, and biodistribution of a novel liposomal emodin, Int. J. Nanomedicine. 7 (2012) 2325– 2337. doi: 10.2147/UN.S31029. 22661889 PMC3357979 · DOI
  73. [78]Zheng C, Ma C, Bai E, Yang K, Xu R, Transferrin and cell-penetrating peptide dual-functioned liposome for targeted drug delivery to glioma, Int. J. Clin. Exp. Med. 8(2015) 1658– 1668. 25932094 PMC4402741
  74. [79]Girão Da Cruz MT, Simões S, Pedroso De Lima MC, Improving lipoplex-mediated gene transfer into C6 glioma cells and primary neurons, Exp. Neurol. 187 (2004) 65– 75. doi: 10.1016/j.expneurol.2003.12.013. 15081589 · DOI
  75. [80]Bartlett DW, Su H, Hildebrandt IJ, Weber WA, Davis ME, Impact of tumor- specific targeting on the biodistribution and efficacy of siRNA nanoparticles measured by multimodality in vivo imaging, Proc. Natl. Acad. Sci. 104 (2007) 15549– 15554. doi: 10.1073/pnas.0707461104. 17875985 PMC1978218 · DOI
  76. [82]Suzuki R, Takizawa T, Kuwata Y, Mutoh M, Ishiguro N, Utoguchi N, Shinohara A, Eriguchi M, Yanagie H, Maruyama K, Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome, Int. J. Pharm. 346 (2008) 143– 150. doi: 10.1016/j.ijpharm.2007.06.010. 17640835 · DOI
  77. [83]Gaillard PJ, Appeldoorn CCM, Dorland R, Van Kregten J, Manca F, Vugts DJ, Windhorst B, Van Dongen GAMS, De Vries HE, Maussang D, Van Tellingen O, Pharmacokinetics, brain delivery, and efficacy in brain tumor-bearing mice of glutathione pegylated liposomal doxorubicin (2B3–101), PLoS One. 9 (2014). doi: 10.1371/journal.pone.0082331. PMC3885379 24416140 · DOI
  78. [84]Johnsen KB, Burkhart A, Melander F, Kempen PJ, Vejlebo JB, Siupka P, Nielsen MS, Andresen TL, Moos T, Targeting transferrin receptors at the blood-brain barrier improves the uptake of immunoliposomes and subsequent cargo transport into the brain parenchyma, Sci. Rep. 7(2017) 1– 13. doi: 10.1038/s41598-017-11220-1. 28871203 PMC5583399 · DOI
  79. [85]Song Q, Huang M, Yao L, Wang X, Gu X, Chen J, Chen J, Huang J, Hu Q, Kang T, Rong Z, Qi H, Zheng G, Chen H, Gao X, Lipoprotein-based nanoparticles rescue the memory loss of mice with alzheimer’s disease by accelerating the clearance of amyloid-beta, ACS Nano. 8 (2014) 2345– 2359. doi: 10.1021/nn4058215. 24527692 · DOI · Paper page
  80. [86]Liu Y, Tseng Y, Huang L, Biodistribution Studies of Nanoparticles Using Fluorescence Imaging: A Qualitative or Quantitative Method?, Pharm. Res. 29 (2012) 3273– 3277. doi: 10.1007/s11095-012-0818-1. 22806405 PMC3584332 · DOI
  81. [87]Knudsen KB, Northeved H, Pramod Kumar EK, Permin A, Gjetting T, Andresen TL, Larsen S, Wegener KM, Lykkesfeldt J, Jantzen K, Loft S, Møller P, Roursgaard M, In vivo toxicity of cationic micelles and liposomes, Nanomedicine Nanotechnology, Biol. Med. 11 (2015) 467– 477. doi: 10.1016/j.nano.2014.08.004. 25168934 · DOI
  82. [88]Gerets HHJ, Hanon E, Cornet M, Dhalluin S, Depelchin O, Canning M, Atienzar FA, Selection of cytotoxicity markers for the screening of new chemical entities in a pharmaceutical context: A preliminary study using a multiplexing approach, Toxicol. Vitr. 23 (2009) 319– 332. doi: 10.1016/j.tiv.2008.11.012. 19110050 · DOI
  83. [89]Campion S, Aubrecht J, Boekelheide K, Brewster DW, Vaidya VS, Anderson L, Burt D, Dere E, Hwang K, Pacheco S, Saikumar J, Schomaker S, Sigman M, Goodsaid F, The current status of biomarkers for predicting toxicity., Expert Opin. Drug Metab. Toxicol. 9 (2013) 1391– 408. doi: 10.1517/17425255.2013.827170. 23961847 PMC3870154 · DOI
  84. [90]Siddiqi NJ, Abdelhalim MAK, El-Ansary AK, Alhomida AS, Ong WY, Identification of potential biomarkers of gold nanoparticle toxicity in rat brains, J. Neuroinflammation. 9 (2012) 656. doi: 10.1186/1742-2094-9-123. PMC3423006 22691312 · DOI
  85. [91]Kawata K, Liu CY, Merkel SF, Ramirez SH, Ryan T, Langford D, Angeles L, Neurosci Biobeha HHS Public Access Author manuscript Published in final edited form as: Blood biomarkers for brain injury: What are we measuring?, Neurosci. Biobehav. Rev 68 (2016) 460– 473. doi: 10.1016/j.neubiorev.2016.05.009.Blood. 27181909 PMC5003664 · DOI
  86. [92]Abu Lila AS, Kiwada H, Ishida T, The accelerated blood clearance (ABC) phenomenon: Clinical challenge and approaches to manage, J. Control. Release 172 (2013) 38– 47. doi: 10.1016/j.jconrel.2013.07.026. 23933235 · DOI · Paper page

Cited by

Sorted by citations

Authors
dos Santos Rodrigues, B., Oue, H., Banerjee, A., Kanekiyo, T., & Singh, J.
Affiliations
  • Mayo Clinic (US)
  • North Dakota State University (US)
Corresponding author
Singh, Jagdish
Venue
Journal of Controlled Release
Publisher
Elsevier BV
Published
2018-09
Volume
286
Pages
264-278
ISSN
0168-3659 (ISSN-L)
OpenAlex
W2887818712
Cited by
116
References
4
Citations by year
2026: 3 · 2025: 10 · 2024: 16 · 2023: 19 · 2022: 22 · 2021: 15 · 2020: 18 · 2019: 12 · 2018: 1
FWCI
4.02
Type
journal article
Language
en
Open access
Locations
  • Journal of Controlled Release (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institutes of Health (R01AG051574)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
  • Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
  • Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Keywords
lipofection, blood-brain barrier, neuronal transfection, transferrin receptor targeting, penetratin, brain accumulation, in vivo transfection, plasmid DNA delivery
MeSH terms
Animals, beta-Galactosidase, Blood-Brain Barrier, Cells, Cultured, DNA, Liposomes, Mice, Inbred C57BL, Neurons, Plasmids, Transfection, Transferrin, Gene Transfer Techniques, Coculture Techniques, Rats, Cell-Penetrating Peptides

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review