CoChat
Sign Up
Cited by 51

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

Comprehensive analysis of the in vitro and ex ovo hemocompatibility of surface engineered iron oxide nanoparticles for biomedical applications

Schlenk, Florian, Werner, Sebastian, Rabel, Martin, Jacobs, Franziska, Bergemann, Christian, Clement, Joachim H., Fischer, Dagmar·2017·Archives of Toxicology
DOI 10.1007/s00204-017-1968-z
Open this paper in CoChat — free account

Abstract

A set of biomedically relevant iron oxide nanoparticles with systematically modified polymer surfaces was investigated regarding their interaction with the first contact partners after systemic administration such as blood cells, blood proteins, and the endothelial blood vessels, to establish structure-activity relationships. All nanoparticles were intensively characterized regarding their physicochemical parameters. Cyto- and hemocompatibility tests showed that (1) the properties of the core material itself were not relevant in short-term incubation studies, and (2) toxicities increased with higher polymer mass, neutral = anionic < cationic surface charge and charge density, as well as agglomeration. Based on this, it was possible to classify the nanoparticles in three groups, to establish structure-activity relationships and to predict nanosafety. While the results between cyto- and hemotoxicity tests correlated well for the polymers, data were not fully transferable for the nanoparticles, especially in case of cationic low molar mass polymer coatings. To evaluate the prediction efficacy of the static in vitro models, the results were compared to those obtained in an ex ovo shell-less hen's egg test after microinjection under dynamic flow conditions. While the polymers demonstrated hemotoxicity profiles comparable to the in vitro tests, the size-dependent risks of nanoparticles could be more efficiently simulated in the more complex ex ovo environment, making the shell-less…

Overview

Integrity signals

Registry

Crossref · 10.1007/s00204-017-1968-z

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Citations

Cites

Show all 3 references

Research works printed but not linked: 73

  1. Ahmad Khanbeigi R, Kumar A, Sadouki F, Lorenz C, Forbes B, Dailey LA, Collins H (2012) The delivered dose: Applying particokinetics to in vitro investigations of nanoparticle internalization by macrophages. J Controll Releas 162:259–266. doi: 10.1016/j.jconrel.2012.07.019 · DOI
  2. Alexiou C, Arnold W, Klein RJ et al (2000) Locoregional cancer treatment with magnetic drug targeting. Cancer Res 60:6641–6648
  3. ASTM (2013) ASTM F756-13, standard practice for assessment of hemolytic properties of materials. ASTM Int doi: 10.1520/F0756 · DOI
  4. Bähring F, Schlenk F, Wotschadlo J et al (2013) Suitability of viability assays for testing biological effects of coated superparamagnetic nanoparticles. IEEE Trans Magn 49:383–388. doi: 10.1109/TMAG.2012.2222635 · DOI
  5. Barrow M, Taylor A, Murray P, Rosseinsky MJ, Adams DJ (2015) Design considerations for the synthesis of polymer coated iron oxide nanoparticles for stem cell labelling and tracking using MRI. Chem Soc Rev 44:6733–6748. doi: 10.1039/C5CS00331H · DOI
  6. Bauer M, Lautenschlaeger C, Kempe K, Tauhardt L, Schubert US, Fischer D (2012) Poly(2-ethyl-2-oxazoline) as alternative for the stealth polymer poly(ethylene glycol): comparison of in vitro cytotoxicity and hemocompatibility. Macromol Biosci 12:986–998. doi: 10.1002/mabi.201200017 · DOI
  7. Bhirde AA, Hassan SA, Harr E, Chen XY (2014) Role of albumin in the formation and stabilization of nanoparticle aggregates in serum studied by continuous photon correlation spectroscopy and multiscale computer simulations. J Phys Chem C 118:16199–16208. doi: 10.1021/jp5034068 · DOI
  8. Briley-Saebo KC, Johansson LO, Hustvedt SO, Haldorsen AG, Bjornerud A, Fayad ZA, Ahlstrom HK (2006) Clearance of iron oxide particles in rat liver: effect of hydrated particle size and coating material on liver metabolism. Invest Radiol 41:560–571. doi: 10.1097/01.rli.0000221321.90261.09 · DOI
  9. Calatayud MP, Sanz B, Raffa V, Riggio C, Ibarra MR, Goya GF (2014) The effect of surface charge of functionalized Fe3O4 nanoparticles on protein adsorption and cell uptake. Biomaterials 35:6389–6399. doi: 10.1016/j.biomaterials.2014.04.009 · DOI
  10. Cardoso AV, Pereira MH, de Araújo Marcondes G, Ferreira AR, de Araújo PR (2007) Microplate reader analysis of triatomine saliva effect on erythrocyte aggregation. Mater Res 10:31–36. doi: 10.1590/S1516-14392007000100008 · DOI
  11. Cedervall T, Lynch I, Lindman S et al (2007) Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc Natl Acad Sci U S A 104:2050–2055. doi: 10.1073/pnas.0608582104 · DOI · Paper page
  12. Choksakulnimitr S, Masuda S, Tokuda H, Takakura Y, Hashida M (1995) In vitro cytotoxicity of macromolecules in different cell culture systems. J Controll Release 34:233–241. doi: 10.1016/0168-3659(95)00007-U · DOI
  13. Chouly C, Pouliquen D, Lucet I, Jeune JJ, Jallet P (1996) Development of superparamagnetic nanoparticles for MRI: effect of particle size, charge and surface nature on biodistribution. J Microencapsul 13:245–255. doi: 10.3109/02652049609026013 · DOI
  14. Clancy AA, Gregoriou Y, Yaehne K, Cramb DT (2010) Measuring properties of nanoparticles in embryonic blood vessels: Towards a physicochemical basis for nanotoxicity. Chem Phys Lett 488:99–111. doi: 10.1016/j.cplett.2010.02.016 · DOI
  15. Cromer Berman SM, Walczak P, Bulte JW (2011) Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip Rev: Nanomed Nanobiotechnol 3:343–355. doi: 10.1002/wnan.140 · DOI
  16. Deng ZJ, Liang M, Toth I, Monteiro M, Minchin RF (2012) Plasma protein binding of positively and negatively charged polymer-coated gold nanoparticles elicits different biological responses. Nanotoxicology 7:314–322. doi: 10.3109/17435390.2012.655342 · DOI
  17. Domey J, Bergemann C, Bremer-Streck S, Krumbein I, Reichenbach JR, Teichgraber U, Hilger I (2015) Long-term prevalence of NIRF-labeled magnetic nanoparticles for the diagnostic and intraoperative imaging of inflammation. Nanotoxicology. doi: 10.3109/17435390.2014.1000413 · DOI
  18. Dunn BE (1974) Technique of shell-less culture of the 72-hour avian embryo. Poult Sci 53:409–412 · DOI
  19. Eberbeck D, Kettering M, Bergemann C, Zirpel P, Hilger I, Trahms L (2010) Quantification of the aggregation of magnetic nanoparticles with different polymeric coatings in cell culture medium. J Phys D: Appl Phys 43:405002. doi: 10.1088/0022-3727/43/40/405002 · DOI
  20. Ehrenberg MS, Friedman AE, Finkelstein JN, Oberdörster G, McGrath JL (2009) The influence of protein adsorption on nanoparticle association with cultured endothelial cells. Biomaterials 30:603–610. doi: 10.1016/j.biomaterials.2008.09.050 · DOI · Paper page
  21. Fernandes JC, Eaton P, Nascimento H et al (2008) Effects of chitooligosaccharides on human red blood cell morphology and membrane protein structure. Biomacromolecules 9:3346–3352. doi: 10.1021/bm800622f · DOI
  22. Fischer D, von Harpe A, Kunath K, Petersen H, Li YX, Kissel T (2002) Copolymers of ethylene imine and N-(2-hydroxyethyl)-ethylene imine as tools to study effects of polymer structure on physicochemical and biological properties of DNA complexes. Bioconjugate Chem 13:1124–1133. doi: 10.1021/bc025550w · DOI
  23. Fischer D, Li Y, Ahlemeyer B, Krieglstein J, Kissel T (2003) In vitro cytotoxicity testing of polycations: influence of polymer structure on cell viability and hemolysis. Biomaterials 24:1121–1131. doi: 10.1016/S0142-9612(02)00445-3 · DOI
  24. Fleischer CC, Payne CK (2014) Nanoparticle–cell interactions: molecular structure of the protein corona and cellular outcomes. Acc Chem Res 47:2651–2659. doi: 10.1021/ar500190q · DOI
  25. Gebauer JS, Malissek M, Simon S et al (2012) Impact of the nanoparticle-protein corona on colloidal stability and protein structure. Langmuir 28:9673–9679. doi: 10.1021/la301104a · DOI
  26. Gessner A, Lieske A, Paulke BR, Müller RH (2002) Influence of surface charge density on protein adsorption on polymeric nanoparticles: analysis by two-dimensional electrophoresis. Eur J Pharm Biopharm 54:165–170. doi: 10.1016/S0939-6411(02)00081-4 · DOI
  27. Ghosh S, Jiang W, McClements JD, Xing B (2011) Colloidal stability of magnetic iron oxide nanoparticles: influence of natural organic matter and synthetic polyelectrolytes. Langmuir 27:8036–8043. doi: 10.1021/la200772e · DOI
  28. Grund S, Bauer M, Fischer D (2011) Polymers in drug delivery—state of the art and future trends. Adv Eng Mater 13:61–87. doi: 10.1002/adem.201080088 · DOI
  29. Grüttner C, Teller J (1999) New types of silica-fortified magnetic nanoparticles as tools for molecular biology applications. J Magn Magn Mater 194:8–15. doi: 10.1016/S0304-8853(98)00561-7 · DOI
  30. Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. Dev Dyn 195:231–272. doi: 10.1002/aja.1001950404 · DOI
  31. Hildebrandt B, Wust P, Ahlers O et al (2002) The cellular and molecular basis of hyperthermia. Crit Rev Oncol Hematol 43:33–56. doi: 10.1016/S1040-8428(01)00179-2 · DOI
  32. Hilger I (2013) In vivo applications of magnetic nanoparticle hyperthermia. Int J Hyperthermia 29:828–834. doi: 10.3109/02656736.2013.832815 · DOI
  33. Hilger I, Kaiser WA (2012) Iron oxide-based nanostructures for MRI and magnetic hyperthermia. Nanomedicine 7:1443–1459. doi: 10.2217/nnm.12.112 · DOI
  34. Hilger I, Andrä W, Hergt R, Hiergeist R, Schubert H, Kaiser WA (2001) Electromagnetic heating of breast tumors in interventional radiology: in vitro and in vivo studies in human cadavers and mice. Radiology 218:570–575. doi: 10.1148/radiology.218.2.r01fe19570 · DOI
  35. Hirsch V, Kinnear C, Moniatte M, Rothen-Rutishauser B, Clift MJ, Fink A (2013) Surface charge of polymer coated SPIONs influences the serum protein adsorption, colloidal stability and subsequent cell interaction in vitro. Nanoscale 5:3723–3732. doi: 10.1039/c2nr33134a · DOI
  36. Jin R, Lin B, Li D, Ai H (2014) Superparamagnetic iron oxide nanoparticles for MR imaging and therapy: design considerations and clinical applications. Curr Opin Pharmacol 18:18–27. doi: 10.1016/j.coph.2014.08.002 · DOI · Paper page
  37. Joris F, Manshian BB, Peynshaert K, De Smedt SC, Braeckmans K, Soenen SJ (2013) Assessing nanoparticle toxicity in cell-based assays: influence of cell culture parameters and optimized models for bridging the in vitro–in vivo gap. Chem Soc Rev 42:8339–8359. doi: 10.1039/c3cs60145e · DOI
  38. Klueh U, Dorsky DI, Moussy F, Kreutzer DL (2003) Ex ova chick chorioallantoic membrane as a novel model for evaluation of tissue responses to biomaterials and implants. J Biomed Mater Res, Part A 67:838–843. doi: 10.1002/jbm.a.10059 · DOI
  39. Landgraf L, Müller I, Ernst P et al (2015) Comparative evaluation of the impact on endothelial cells induced by different nanoparticle structures and functionalization. Beilstein J Nanotechnol 6:300–312. doi: 10.3762/bjnano.6.28 · DOI
  40. Ludwig R, Stapf M, Dutz S, Muller R, Teichgraber U, Hilger I (2014) Structural properties of magnetic nanoparticles determine their heating behavior—an estimation of the in vivo heating potential. Nanoscale Res Lett 9(1):602. doi: 10.1186/1556-276X-9-602 · DOI
  41. Ma Z, Bai J, Wang Y, Jiang X (2014) Impact of shape and pore size of mesoporous silica nanoparticles on serum protein adsorption and RBCs hemolysis. ACS Appl Mater Interfaces 6:2431–2438. doi: 10.1021/am404860q · DOI
  42. Maffre P, Brandholt S, Nienhaus K, Shang L, Parak WJ, Nienhaus GU (2014) Effects of surface functionalization on the adsorption of human serum albumin onto nanoparticles—a fluorescence correlation spectroscopy study. Beilstein J Nanotechnol 5:2036–2047. doi: 10.3762/bjnano.5.212 · DOI
  43. Mahmoudi M, Hofmann H, Rothen-Rutishauser B, Petri-Fink A (2012) Assessing the in vitro and in vivo toxicity of superparamagnetic iron oxide nanoparticles. Chem Rev 112:2323–2338. doi: 10.1021/Cr2002596 · DOI
  44. Monopoli MP, Åberg C, Salvati A, Dawson KA (2012) Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol 7:779–786. doi: 10.1038/nnano.2012.207 · DOI · Paper page
  45. Mosesson MW (2005) Fibrinogen and fibrin structure and functions. J Thromb Haemost 3:1894–1904. doi: 10.1111/j.1538-7836.2005.01365.x · DOI · Paper page
  46. Müller R, Stranik O, Schlenk F, Werner S, Malsch D, Fischer D, Fritzsche W (2015) Optical detection of nanoparticle agglomeration in a living system under the influence of a magnetic field. J Magn Magn Mater 380:61–65. doi: 10.1016/j.jmmm.2014.10.043 · DOI
  47. Neu B, Wenby R, Meiselman HJ (2008) Effects of dextran molecular weight on red blood cell aggregation. Biophys J 95:3059–3065. doi: 10.1529/biophysj.108.130328 · DOI
  48. Olsvik Ø, Popovic T, Skjerve E, Cudjoe KS, Hornes E, Ugelstad J, Uhlén M (1994) Magnetic separation techniques in diagnostic microbiology. Clin Microbiol Rev 7:43–54 · DOI
  49. Öztürk N, Bereli N, Akgöl S, Denizli A (2008) High capacity binding of antibodies by poly(hydroxyethyl methacrylate) nanoparticles. Colloids Surf, B 67:14–19. doi: 10.1016/j.colsurfb.2008.07.005 · DOI
  50. Peng Q, Zhang S, Yang Q et al (2013) Preformed albumin corona, a protective coating for nanoparticles based drug delivery system. Biomaterials 34:8521–8530. doi: 10.1016/j.biomaterials.2013.07.102 · DOI · Paper page
  51. Perez JM, Josephson L, O’Loughlin T, Högemann D, Weissleder R (2002) Magnetic relaxation switches capable of sensing molecular interactions. Nat Biotechnol 20:816–820. doi: 10.1038/nbt720 · DOI
  52. Rajan B, Sathish S, Balakumar S, Devaki T (2015) Synthesis and dose interval dependent hepatotoxicity evaluation of intravenously administered polyethylene glycol-8000 coated ultra-small superparamagnetic iron oxide nanoparticle on Wistar rats. Environ Toxicol Pharmacol 39:727–735. doi: 10.1016/j.etap.2015.01.018 · DOI
  53. Reddy LH, Arias JL, Nicolas J, Couvreur P (2012) Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chem Rev 112:5818–5878. doi: 10.1021/cr300068p · DOI · Paper page
  54. Reimer P, Balzer T (2003) Ferucarbotran (Resovist): a new clinically approved RES-specific contrast agent for contrast-enhanced MRI of the liver: properties, clinical development, and applications. Eur Radiol 13:1266–1276. doi: 10.1007/s00330-002-1721-7 · DOI · Paper page
  55. Röcker C, Pötzl M, Zhang F, Parak WJ, Nienhaus GU (2009) A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat Nanotechnol 4:577–580. doi: 10.1038/nnano.2009.195 · DOI
  56. Rosenbruch M (1994) Early stages of the incubated chicken egg as a model in experimental biology and medicine. ALTEX 11:199–206
  57. Santhosh PB, Ulrih NP (2013) Multifunctional superparamagnetic iron oxide nanoparticles: promising tools in cancer theranostics. Cancer Lett 336:8–17. doi: 10.1016/j.canlet.2013.04.032 · DOI · Paper page
  58. Saraswathy A, Nazeer SS, Nimi N, Arumugam S, Shenoy SJ, Jayasree RS (2014) Synthesis and characterization of dextran stabilized superparamagnetic iron oxide nanoparticles for in vivo MR imaging of liver fibrosis. Carbohydr Polym 101:760–768. doi: 10.1016/j.carbpol.2013.10.015 · DOI
  59. Schlenk F, Grund S, Fischer D (2013) Recent developments and perspectives on gene therapy using synthetic vectors. Ther Deliv 4:95–113. doi: 10.4155/tde.12.128 · DOI
  60. Schroeder HW, Cavacini L (2010) Structure and function of immunoglobulins. J Allergy Clin Immunol 125:41–52. doi: 10.1016/j.jaci.2009.09.046 · DOI
  61. Setyawati MI, Tay CY, Docter D, Stauber RH, Leong DT (2015) Understanding and exploiting nanoparticles’ intimacy with the blood vessel and blood. Chem Soc Rev 44:8174–8199. doi: 10.1039/c5cs00499c · DOI
  62. Stins MF, Badger J, Kim KS (2001) Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb Pathogenesis 30:19–28. doi: 10.1006/mpat.2000.0406 · DOI
  63. Subramanian A, Rau AV, Kaligotla H (2006) Surface modification of chitosan for selective surface-protein interaction. Carbohydr Polym 66:321–332. doi: 10.1016/j.carbpol.2006.03.022 · DOI
  64. Tenzer S, Docter D, Kuharev J et al (2013) Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat Nanotechnol 8:772–781. doi: 10.1038/nnano.2013.181 · DOI · Paper page
  65. Vargas A, Zeisser-Labouèbe M, Lange N, Gurny R, Delie F (2007) The chick embryo and its chorioallantoic membrane (CAM) for the in vivo evaluation of drug delivery systems. Adv Drug Deliv Rev 59:1162–1176. doi: 10.1016/j.addr.2007.04.019 · DOI
  66. Verma A, Stellacci F (2010) Effect of surface properties on nanoparticle–cell interactions. Small 6:12–21. doi: 10.1002/smll.200901158 · DOI
  67. Wang YX (2011) Superparamagnetic iron oxide based MRI contrast agents: current status of clinical application. Quant Imaging Med Surg 1:35–40. doi: 10.3978/j.issn.2223-4292.2011.08.03 · DOI
  68. Wen G, Zhang XL, Chang RM, Xia Q, Cang P, Zhang Y (2002) Superparamagnetic iron oxide (Feridex)-enhanced MRI in diagnosis of focal hepatic lesions. Di Yi Jun Yi Da Xue Xue Bao 22:451–452
  69. Woodard H, White D (1986) The composition of body tissues. Br J Radiol 59:1209–1218. doi: 10.1259/0007-1285-59-708-1209 · DOI
  70. Yaehne K, Tekrony A, Clancy A et al (2013) Nanoparticle accumulation in angiogenic tissues: towards predictable pharmacokinetics. Small 9:3118–3127. doi: 10.1002/smll.201201848 · DOI
  71. Zhao M, Josephson L, Tang Y, Weissleder R (2003) Magnetic sensors for protease assays. Angew Chem Int Ed 42:1375–1378. doi: 10.1002/anie.200390352 · DOI
  72. Zhu M, Nie G, Meng H, Xia T, Nel A, Zhao Y (2012) Physicochemical properties determine nanomaterial cellular uptake, transport, and fate. Acc Chem Res 46:622–631. doi: 10.1021/ar300031y · DOI
  73. Zwadlo-Klarwasser G, Görlitz K, Hafemann B, Klee D, Klosterhalfen B (2001) The chorioallantoic membrane of the chick embryo as a simple model for the study of the angiogenic and inflammatory response to biomaterials. J Mater Sci: Mater Med 12:195–199. doi: 10.1023/A:1008950713001 · DOI

Cited by

Sorted by citations

Metadata

Authors
Schlenk, F., Werner, S., Rabel, M., Jacobs, F., Bergemann, C., Clement, J. H., & Fischer, D.
Venue
Archives of Toxicology
Publisher
Springer Science and Business Media LLC
Published
2017-04-04
Volume
91
Issue
10
Pages
3271-3286
ISSN
  • 0340-5761
  • 1432-0738
DOI
10.1007/s00204-017-1968-z
Cited by
51
References
3
Language
en
Licence
www.springer.com/tdm (unspecified)
Funders
BMBF (03X0104, 03XP0003)

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