CoChat
Sign Up
Cited by 47Nanoparticle-Based Drug DeliveryRadiopharmaceutical Chemistry and ApplicationsNanoplatforms for cancer theranostics

The DOI matches its Crossref record.

Red Blood Cell Membrane Bioengineered Zr-89 Labelled Hollow Mesoporous Silica Nanosphere for Overcoming Phagocytosis

Open access
Lee, Jun Young, Vyas, Chirag K., Kim, Gun Gyun, Choi, Pyeong Seok, Hur, Min Goo, Yang, Seung Dae, Kong, Young Bae, Lee, Eun Je, Park, Jeong Hoon·2019·Scientific Reports
DOI 10.1038/s41598-019-43969-yPMC PMC6520393
Open this paper in CoChat — free accountOpen PDF

Abstract

Abstract Biomimetic nanoparticles (NPs) have been actively studied for their biological compatibility due to its distinguished abilities viz. long-term circulation, low toxicity, ease for surface modification, and its ability to avoid phagocytosis of NPs by macrophages. Coating the NPs with a variety of cell membranes bearing the immune control proteins increases drug efficacy while complementing the intrinsic advantages of the NPs. In this study, efforts were made to introduce oxophilic radiometal 89Zr with hollow mesoporous silica nanospheres (HMSNs) having abundant silanol groups and were bioengineered with red blood cell membrane (Rm) having cluster of differentiation 47 (CD47) protein to evaluate its long-term in vivo behavior. We were successful in demonstrating the increased in vivo stability of synthesized Rm-camouflaged, 89Zr-labelled HMSNs with the markedly reduced 89Zr release. Rm camouflaged 89Zr-HMSNs effectively accumulated in the tumor by avoiding phagocytosis of macrophages. In addition, re-injecting the Rm isolated using the blood of the same animal helped to overcome the immune barrier. This novel strategy can be applied extensively to identify the long-term in vivo behavior of nano-drugs while enhancing their biocompatibility.

Overview

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 · 10.1038/s41598-019-43969-y

Cites

Statistics

Figures

Figure 1 Stepwise representation of the synthesis of Rm-camouflaged 89Zr-labelled HMSNs. First, blood collection by <10% circulating blood volume from the mouse and second, re-injection for overcoming the immune barrier.
Figure 1 Stepwise representation of the synthesis of Rm-camouflaged 89Zr-labelled HMSNs. First, blood collection by <10% circulating blood volume from the mouse and second, re-injection for overcoming the immune barrier.CC BY · PubMed Central
Figure 2 Representative SEM (A) and TEM (B–E) images of biomimetic nanoparticles; (A) HMSNs (B) Mesoporous silica nanoparticles coated SNP (C) HMSNs (D) Rm-HMSNs, and (E) Rm ghost with differently scale bar.
Figure 2 Representative SEM (A) and TEM (B–E) images of biomimetic nanoparticles; (A) HMSNs (B) Mesoporous silica nanoparticles coated SNP (C) HMSNs (D) Rm-HMSNs, and (E) Rm ghost with differently scale bar.CC BY · PubMed Central
Figure 3 Physicochemical characterization. (A) Hydrodynamic size (top: blue bar) and Zeta Potential (bottom: pink bar) of SNP, Rm-SNP, HMSN, and Rm-HMSN (n = 3; mean ± s.d.). (B) The photographs of dispersion of the SNP, Rm-SNP, HMSN, and Rm-HMSN (500 µL, 1.0 mg/mL).
Figure 3 Physicochemical characterization. (A) Hydrodynamic size (top: blue bar) and Zeta Potential (bottom: pink bar) of SNP, Rm-SNP, HMSN, and Rm-HMSN (n = 3; mean ± s.d.). (B) The photographs of dispersion of the SNP, Rm-SNP, HMSN, and Rm-HMSN (500 µL, 1.0 mg/mL).CC BY · PubMed Central
Figure 4 Proteins characterization of relative RBC membrane. (A) SDS-PAGE and Western blotting protein analysis of RBC ghost and Rm-HMSN (B) Expression levels of CD47 protein on RBC Ghost and Rm-HMSN.
Figure 4 Proteins characterization of relative RBC membrane. (A) SDS-PAGE and Western blotting protein analysis of RBC ghost and Rm-HMSN (B) Expression levels of CD47 protein on RBC Ghost and Rm-HMSN.CC BY · PubMed Central
Figure 5 (A) Biodistribution study of Rm-89Zr-HMSNs in CT-26 tumor-bearing female Balb/c mice (n = 3 per group). (B) Small animal PET images of CT-26 tumor-bearing female Balb/c mice with 89Zr-HMSNs (top), Rm-89Zr-SNPs (middle) and Rm-89Zr-HMSNs (bottom). PET images were obtained for 1 week after tail intravenous injection of 89Zr labelled NPs.
Figure 5 (A) Biodistribution study of Rm-89Zr-HMSNs in CT-26 tumor-bearing female Balb/c mice (n = 3 per group). (B) Small animal PET images of CT-26 tumor-bearing female Balb/c mice with 89Zr-HMSNs (top), Rm-89Zr-SNPs (middle) and Rm-89Zr-HMSNs (bottom). PET images were obtained for 1 week after tail intravenous injection of 89Zr labelled NPs.CC BY · PubMed Central
Figure 6 In vivo; Blood clearance curves were obtained for 54 hour after tail intravenous injection of 89Zr labelled NPs (n = 3; mean ± s.d.).
Figure 6 In vivo; Blood clearance curves were obtained for 54 hour after tail intravenous injection of 89Zr labelled NPs (n = 3; mean ± s.d.).CC BY · PubMed Central

Verification

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?

Self-check

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

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

Citations

Cites

Still being checked.

Research works printed but not linked: 52

  1. Honary, S. & Zahir, F. In Tropical Journal of Pharmaceutical Research Vol. 12, 255–264 (2013). · DOI
  2. He, C., Hu, Y., Yin, L., Tang, C. & Yin, C. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 31, 3657–3666 (2010). · DOI · Paper page
  3. Oh, N. & Park, J.-H. Endocytosis and exocytosis of nanoparticles in mammalian cells. International journal of nanomedicine 9, 51 (2014).
  4. Yu, T., Hubbard, D., Ray, A. & Ghandehari, H. In vivo biodistribution and pharmacokinetics of silica nanoparticles as a function of geometry, porosity and surface characteristics. Journal of controlled release 163, 46–54 (2012). · DOI
  5. Tang, L. & Cheng, J. Nonporous silica nanoparticles for nanomedicine application. Nano today 8, 290–312 (2013). · DOI
  6. Watermann, A. & Brieger, J. Mesoporous silica nanoparticles as drug delivery vehicles in cancer. Nanomaterials 7, 189 (2017). · DOI
  7. Wani, A. et al. Surface PEGylation of Mesoporous Silica Nanorods (MSNR): Effect on loading, release, and delivery of mitoxantrone in hypoxic cancer cells. Scientific reports 7, 2274 (2017). · DOI
  8. Eshete, M., Bailey, K., Nguyen, T. D. T., Aryal, S. & Choi, S.-O. Interaction of Immune System Protein with PEGylated and Un-PEGylated Polymeric Nanoparticles. Advances in Nanoparticles 6, 103 (2017). · DOI
  9. Suk, J. S., Xu, Q., Kim, N., Hanes, J. & Ensign, L. M. PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Advanced drug delivery reviews 99, 28–51 (2016). · DOI · Paper page
  10. Lázaro, I. A. et al. Selective Surface PEGylation of UiO-66 Nanoparticles for Enhanced Stability, Cell Uptake, and pH-Responsive. Drug Delivery. Chem 2, 561–578 (2017).
  11. Su, J. et al. Long Circulation Red‐Blood‐Cell‐Mimetic Nanoparticles with Peptide‐Enhanced Tumor Penetration for Simultaneously Inhibiting Growth and Lung Metastasis of Breast Cancer. Advanced Functional Materials 26, 1243–1252 (2016). · DOI
  12. Hu, C.-M. J. et al. Marker-of-self functionalization of nanoscale particles through a top-down cellular membrane coating approach. Nanoscale 5, 2664–2668 (2013). · DOI
  13. Zhai, Y. et al. Preparation and application of cell membrane-camouflaged nanoparticles for cancer therapy. Theranostics 7, 2575 (2017). · DOI
  14. Rao, L. et al. Red blood cell membrane as a biomimetic nanocoating for prolonged circulation time and reduced accelerated blood clearance. Small 11, 6225–6236 (2015). · DOI
  15. Tárnok, A. Flow and image cytometry side by side for the new frontiers in quantitative single‐cell analysis. Cytometry Part A: The Journal of the International Society for Advancement of Cytometry 75, 169–171 (2009). · DOI
  16. Huang, Y. X. et al. Restoring the youth of aged red blood cells and extending their lifespan in circulation by remodelling membrane sialic acid. Journal of cellular and molecular medicine 20, 294–301 (2016). · DOI
  17. Khandelwal, S., Van Rooijen, N. & Saxena, R. K. Reduced expression of CD47 during murine red blood cell (RBC) senescence and its role in RBC clearance from the circulation. Transfusion 47, 1725–1732 (2007). · DOI
  18. Tsai, R. K., Rodriguez, P. L. & Discher, D. E. Self inhibition of phagocytosis: the affinity of ‘marker of self’ CD47 for SIRPα dictates potency of inhibition but only at low expression levels. Blood Cells, Molecules, and Diseases 45, 67–74 (2010). · DOI
  19. Qie, Y. et al. Surface modification of nanoparticles enables selective evasion of phagocytic clearance by distinct macrophage phenotypes. Scientific reports 6, 26269 (2016). · DOI
  20. Zheleznyak, A. et al. Imaging of CD47 Expression in Xenograft and Allograft Tumor Models. Molecular Imaging 12, 1–10 (2013). · DOI
  21. Willingham, S. B. et al. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proceedings of the National Academy of Sciences 109, 6662–6667 (2012). · DOI
  22. Shi, S., Chen, F. & Cai, W. Biomedical applications of functionalized hollow mesoporous silica nanoparticles: focusing on molecular imaging. Nanomedicine 8, 2027–2039 (2013). · DOI
  23. Chen, Y., Chen, H.-R. & Shi, J.-L. Construction of homogenous/heterogeneous hollow mesoporous silica nanostructures by silica-etching chemistry: principles, synthesis, and applications. Accounts of chemical research 47, 125–137 (2013). · DOI
  24. Li, M., Zhang, C., Yang, X.-L. & Xu, H.-B. Controllable synthesis of hollow mesoporous silica nanoparticles templated by kinetic self-assembly using a gemini surfactant. RSC Advances 3, 16304–16307 (2013). · DOI
  25. Lee, S. B. et al. Mesoporous Silica Nanoparticle Pretargeting for PET Imaging Based on a Rapid Bioorthogonal Reaction in a Living Body. Angewandte Chemie 52, 10549–10552 (2013). · DOI
  26. Chen, F. et al. Engineering of hollow mesoporous silica nanoparticles for remarkably enhanced tumor active targeting efficacy. Scientific reports 4, 5080 (2014). · DOI
  27. Li, Y. et al. Hollow mesoporous silica nanoparticles with tunable structures for controlled drug delivery. ACS applied materials & interfaces 9, 2123–2129 (2017). · DOI
  28. Kamkaew, A. et al. Cerenkov radiation induced photodynamic therapy using chlorin e6-loaded hollow mesoporous silica nanoparticles. ACS applied materials & interfaces 8, 26630–26637 (2016). · DOI
  29. Chen, F. et al. In vivo integrity and biological fate of chelator-free zirconium-89-labelled mesoporous silica nanoparticles. ACS nano 9, 7950–7959 (2015). · DOI
  30. Shaffer, T. M. et al. Silica nanoparticles as substrates for chelator-free labeling of oxophilic radioisotopes. Nano letters 15, 864–868 (2015). · DOI
  31. O’Farrell, A., Shnyder, S., Marston, G., Coletta, P. & Gill, J. Non‐invasive molecular imaging for preclinical cancer therapeutic development. British journal of pharmacology 169, 719–735 (2013). · DOI
  32. Buck, A. K. et al. Economic evaluation of PET and PET/CT in oncology: evidence and methodologic approaches. Journal of nuclear medicine technology 38, 6–17 (2010). · DOI
  33. Wadas, T. J., Wong, E. H., Weisman, G. R. & Anderson, C. J. Coordinating radiometals of copper, gallium, indium, yttrium, and zirconium for PET and SPECT imaging of disease. Chemical reviews 110, 2858–2902 (2010). · DOI
  34. Holland, J. P., Williamson, M. J. & Lewis, J. S. Unconventional nuclides for radiopharmaceuticals. Molecular imaging 9, 7290.2010. 00008 (2010). · DOI
  35. Holland, J. P., Sheh, Y. & Lewis, J. S. Standardized methods for the production of high specific-activity zirconium-89. Nuclear medicine and biology 36, 729–739 (2009). · DOI
  36. Fang, X., Chen, C., Liu, Z., Liu, P. & Zheng, N. A cationic surfactant assisted selective etching strategy to hollow mesoporous silica spheres. Nanoscale 3, 1632–1639 (2011). · DOI
  37. Dean, J. A. Lange’s handbook of chemistry. Material and manufacturing process 5, 687–688 (1990). · DOI
  38. Kim, T.-H., Lee, J. Y., Kim, M.-K., Park, J. H. & Oh, J.-M. Radioisotope Co-57 incorporated layered double hydroxide nanoparticles as a cancer imaging agent. RSC Advances 6, 48415–48419 (2016). · DOI
  39. Liang, S., Jin, X., Ma, Y., Guo, J. & Wang, H. Folic acid-conjugated BSA nanocapsule (n-BSA–FA) for cancer targeted radiotherapy and imaging. RSC Advances 5, 88560–88566 (2015). · DOI
  40. Kong, M. et al. Biodegradable hollow mesoporous silica nanoparticles for regulating tumor microenvironment and enhancing antitumor efficiency. Theranostics 7, 3276 (2017). · DOI · Paper page
  41. Tian, Y. et al. Redox stimuli-responsive hollow mesoporous silica nanocarriers for targeted drug delivery in cancer therapy. Nanoscale Horizons 1, 480–487 (2016). · DOI
  42. Baas, J., Senninger, N. & Elser, H. The reticuloendothelial system. An overview of function, pathology and recent methods of measurement. Zeitschrift fur Gastroenterologie 32, 117–123 (1994).
  43. Tsai, R. K. & Discher, D. E. Inhibition of “self” engulfment through deactivation of myosin-II at the phagocytic synapse between human cells. The Journal of cell biology 180, 989–1003 (2008). · DOI · Paper page
  44. Gardai, S. J. et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321–334 (2005). · DOI · Paper page
  45. Gustafson, H. H., Holt-Casper, D., Grainger, D. W. & Ghandehari, H. Nanoparticle uptake: the phagocyte problem. Nano today 10, 487–510 (2015). · DOI
  46. Hak, S. et al. The effect of nanoparticle polyethylene glycol surface density on ligand-directed tumor targeting studied in vivo by dual modality imaging. ACS nano 6, 5648–5658 (2012). · DOI
  47. Jauw, Y. W. et al. Immuno-positron emission tomography with zirconium-89-labelled monoclonal antibodies in oncology: what can we learn from initial clinical trials? Frontiers in pharmacology 7, 131 (2016). · DOI
  48. Kasbollah, A., Eu, P., Cowell, S. & Deb, P. Review on production of 89Zr in a medical cyclotron for PET radiopharmaceuticals. Journal of nuclear medicine technology, jnmt. 112.111377 (2013). · DOI
  49. Van de Watering, F. C. et al. Zirconium-89 labelled antibodies: a new tool for molecular imaging in cancer patients. BioMed research international 2014 (2014). · DOI
  50. Vera, D. R. B. et al. Immuno-PET imaging of tumor-infiltrating lymphocytes using zirconium-89 radiolabelled anti-CD3 antibody in immune-competent mice bearing syngeneic tumors. PloS one 13, e0193832 (2018). · DOI
  51. Stöber, W., Fink, A. & Bohn, E. Controlled growth of monodisperse silica spheres in the micron size range. Journal of colloid and interface science 26, 62–69 (1968). · DOI
  52. Liu, J. et al. Hollow mesoporous silica nanoparticles facilitated drug delivery via cascade pH stimuli in tumor microenvironment for tumor therapy. Biomaterials 83, 51–65 (2016). · DOI

Cited by

Sorted by citations

Metadata

Authors
Lee, J. Y., Vyas, C. K., Kim, G. G., Choi, P. S., Hur, M. G., Yang, S. D., Kong, Y. B., Lee, E. J., & Park, J. H.
Affiliations
Korea Atomic Energy Research Institute (KR)
Corresponding author
Park, Jeong Hoon
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2019-05-15
Volume
9
Issue
1
Pages
7419-7419
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-019-43969-y
PMC
PMC6520393
OpenAlex
W2946219025
Cited by
47
References
0
Citations by year
2026: 2 · 2025: 6 · 2024: 6 · 2023: 6 · 2022: 7 · 2021: 9 · 2020: 9 · 2019: 2
FWCI
1.91
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
National Research Foundation of Korea (2018M2A2B3A02071348, 2017M2A2A6A05016600)
Topics
  • Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Radiopharmaceutical Chemistry and Applications
  • Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
Keywords
erythrocyte membrane, biomimetic nanoparticles, CD47, macrophage recognition, tumor accumulation, radiopharmaceuticals, in vivo stability, immune evasion, silanol groups
MeSH terms
Animals, Erythrocyte Membrane, Female, Mice, Inbred BALB C, Phagocytosis, Radioisotopes, Silicon Dioxide, Zirconium, Biomimetic Materials, Cell Line, Tumor, Mice, Nanospheres, Bioengineering

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