journal article·2021Open access

The detrimental invasiveness of glioma cells controlled by gadolinium chelate-coated gold nanoparticles

Maxime Durand, Elodie Lelievre, Alicia Chateau, Alexandre Berquand, Gautier Laurent, Philippe Carl, Stéphane Roux, Lise Chazee, Rana Bazzi, Frederic Eghiaian, Justine Jubreaux, Philippe Ronde, Muriel Barberi-Heyob, Pascal Chastagner, Jérôme Devy, Sophie Pinel

Nanoscale· Volume 13· Issue 20

Abstract

Glioblastoma are characterized by an invasive phenotype, which is thought to be responsible for recurrences and the short overall survival of patients. In the last decade, the promising potential of ultrasmall gadolinium chelate-coated gold nanoparticles (namely Au@DTDTPA(Gd)) was evidenced for image-guided radiotherapy in brain tumors. Considering the threat posed by invasiveness properties of glioma cells, we were interested in further investigating the biological effects of Au@DTDTPA(Gd) by examining their impact on GBM cell migration and invasion. In our work, exposure of U251 glioma cells to Au@DTDTPA(Gd) led to high accumulation of gold nanoparticles, that were mainly diffusely distributed in the cytoplasm of the tumor cells. Experiments pointed out a significant decrease in glioma cell invasiveness when exposed to nanoparticles. As the proteolysis activities were not directly affected by the intracytoplasmic accumulation of Au@DTDTPA(Gd), the anti-invasive effect cannot be attributed to matrix remodeling impairment. Rather, Au@DTDTPA(Gd) nanoparticles affected the intrinsic biomechanical properties of U251 glioma cells, such as cell stiffness, adhesion and generated traction forces, and significantly reduced the formation of protrusions, thus exerting an inhibitory effect on their migration capacities. Consistently, analysis of talin-1 expression and membrane expression of beta 1 integrin evoke the stabilization of focal adhesion plaques in the presence of nanoparticles. Taken together, our results highlight the interest in Au@DTDTPA(Gd) nanoparticles for the therapeutic management of astrocytic tumors, not only as a radio-enhancing agent but also by reducing the invasive potential of glioma cells.
Source: openalex_inverted_index · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Nanoparticle-Based Drug Delivery · Cellular Mechanics and Interactions · Nanoplatforms for cancer theranostics

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Université de Lorraine

CNRS

CRAN

F-54000 Nancy

France

Université de Reims-Champagne-Ardennes

UMR CNRS/URCA 7369

MEDyC

F-51100 Reims

EA 4682

Université Bourgogne Franche-Comté

UMR CNRS 6213-UBFC

UTINAM

F-25000 Besançon

Université de Strasbourg

CNRS UMR 7021 – Strasbourg

Abberior Instruments GmbH

F-13008 Marseille

References (54)

Show source-provided references
1. Alieva · Sci. Rep. · 2019 · 9 · 205410.1038/s41598-019-38625-4 ↗
2. Pinel · Adv. Drug Delivery Rev. · 2019 · 138 · 34410.1016/j.addr.2018.10.013 ↗
3. Alric · Nanoscale · 2013 · 5 · 593010.1039/C3NR00012E ↗
4. McMahon · Sci. Rep. · 2011 · 1 · 1810.1038/srep00018 ↗
5. Miladi · Small · 2014 · 10 · 111610.1002/smll.201302303 ↗
6. Pernodet · Small · 2006 · 2 · 76610.1002/smll.200500492 ↗
7. Arvizo · Proc. Natl. Acad. Sci. U. S. A. · 2013 · 110 · 670010.1073/pnas.1214547110 ↗
8. Li · Int. J. Nanomed. · 2017 · 12 · 350910.2147/IJN.S128802 ↗
9. Chithrani · Nano Lett. · 2006 · 6 · 66210.1021/nl052396o ↗
10. Chithrani · Nano Lett. · 2007 · 7 · 154210.1021/nl070363y ↗
11. Huang · ACS Nano · 2012 · 6 · 448310.1021/nn301282m ↗
12. Jiang · Nat. Nanotechnol. · 2008 · 3 · 14510.1038/nnano.2008.30 ↗
13. Chithrani · Radiat. Res. · 2010 · 173 · 71910.1667/RR1984.1 ↗
14. C. Boyoglu , Q.He , G.Willing , S.Boyoglu-Barnum , V. A.Dennis , S.Pillai and S. R.Singh , Microscopic Studies of Various Sizes of Gold Nanoparticles and Their Cellular Localizations https://www.hindawi.com/journals/isrn/2013/123838/ (accessed Sep 21, 2020). DOI: 10.1155/2013/12383810.1155/2013/123838 ↗
15. Chuang · Biochim. Biophys. Acta, Gen. Subj. · 2013 · 1830 · 496010.1016/j.bbagen.2013.06.025 ↗
16. Xia · Int. J. Nanomed. · 2019 · 14 · 695710.2147/IJN.S214008 ↗
17. Hou · Int. J. Nanomed. · 2013 · 8 · 361910.2147/IJN.S38992 ↗
18. Fayzullin · Transl. Oncol. · 2019 · 12 · 12210.1016/j.tranon.2018.09.014 ↗
19. Vinci · J. Vis. Exp. · 2015 · 99 · e5268610.3791/52686 ↗
20. Tevis · Adv. Biosyst. · 2017 · 1 · 170008310.1002/adbi.201700083 ↗
21. Jiménez Sánchez · Int. J. Mol. Sci. · 2019 · 20 · 461810.3390/ijms20184618 ↗
22. Zhou · Adv. Funct. Mater. · 2014 · 24 · 692210.1002/adfm.201401642 ↗
23. Shin · Int. J. Nanomed. · 2018 · 13 · 329510.2147/IJN.S158463 ↗
24. Cuddapah · Nat. Rev. Neurosci. · 2014 · 15 · 45510.1038/nrn3765 ↗
25. Roomi · Int. J. Oncol. · 2014 · 45 · 88710.3892/ijo.2014.2465 ↗
26. Forsyth · Br. J. Cancer · 1999 · 79 · 182810.1038/sj.bjc.6990291 ↗
27. F. Liu , D.Ma , W.Chen , X.Chen , Y.Qian , Y.Zhao , T.Hu , R.Yin , Y.Zhu , Y.Zhang , Y.Zhang and W.Zhao , Gold Nanoparticles Suppressed Proliferation, Migration, and Invasion in Papillary Thyroid Carcinoma Cells via Downregulation of CCT3 https://www.hindawi.com/journals/jnm/2019/1687340/ (accessed Sep 21, 2020). DOI: 10.1155/2019/168734010.1155/2019/1687340 ↗
28. Hagemann · World J. Cancer Res · 2012 · 3 · 6710.5306/wjco.v3.i5.67 ↗
29. Rao · Nat. Rev. Cancer · 2003 · 3 · 48910.1038/nrc1121 ↗
30. Friedl · Nat. Rev. Cancer · 2003 · 3 · 36210.1038/nrc1075 ↗
31. Jonkman · Cell Adh. Migr. · 2014 · 8 · 44010.4161/cam.36224 ↗
32. Jain · J. Vis. Exp. · 2012 · 63 · e358510.3791/3585 ↗
33. Li · Artif. Cells, Nanomed., Biotechnol. · 2019 · 47 · 302910.1080/21691401.2019.1642902 ↗
34. Shahhoseini · Int. J. Mol. Sci. · 2019 · 20 · 448810.3390/ijms20184488 ↗
35. Xu · Cancer · 2020 · 12 · 166710.3390/cancers12061667 ↗
36. Pontes · J. Cell Biol. · 2017 · 216 · 295910.1083/jcb.201611117 ↗
37. Septiadi · Adv. Mater. · 2018 · 30 · 170446310.1002/adma.201704463 ↗
38. Mulens-Arias · Biomater. Sci. · 2018 · 7 · 38910.1039/C8BM01267A ↗
39. Fang · Asian Pac. J. Cancer Prev. · 2014 · 15 · 265510.7314/apjcp.2014.15.6.2655 ↗
40. Kraning-Rush · PLoS One · 2012 · 7 · e3257210.1371/journal.pone.0032572 ↗
41. Plotnikov · Methods Cell Biol. · 2014 · 123 · 36710.1016/B978-0-12-420138-5.00020-3 ↗
42. Tanner · APL Bioeng. · 2018 · 2 · 03180110.1063/1.5024394 ↗
43. Tay · Nano Lett. · 2014 · 14 · 8310.1021/nl4032549 ↗
44. Osswald · Nature · 2015 · 528 · 9310.1038/nature16071 ↗
45. Weil · Neuro-Oncology · 2017 · 19 · 131610.1093/neuonc/nox070 ↗
46. Debouttière · Adv. Funct. Mater. · 2006 · 16 · 233010.1002/adfm.200600242 ↗
47. Alric · J. Am. Chem. Soc. · 2008 · 130 · 590810.1021/ja078176p ↗
48. Schloetel · Sci. Rep. · 2019 · 9 · 467410.1038/s41598-019-40718-z ↗
49. Theret · Oncotarget · 2017 · 8 · 7861410.18632/oncotarget.20201 ↗
50. Huang · Sci. Rep. · 2019 · 9 · 53910.1038/s41598-018-36896-x ↗
51. Yeung · Cell Motil. · 2005 · 60 · 2410.1002/cm.20041 ↗
52. Munthe · J. Neuro-Oncol. · 2016 · 130 · 5310.1007/s11060-016-2221-y ↗
53. Broekman · Nat. Rev. Neurol. · 2018 · 14 · 48210.1038/s41582-018-0025-8 ↗
54. Vollmann-Zwerenz · Int. J. Mol. Sci. · 2020 · 21 · 193210.3390/ijms21061932 ↗