Dose-response of superparamagnetic iron oxide labeling on mesenchymal stem cells chondrogenic differentiation: A multi-scale in vitro study

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Roeder, Emilie ^a   Henrionnet, Christel ^a   Goebel, Jean Christophe ^b   Gambier, Nicolas ^a   Beuf, Olivier ^b   Grenier, Denis ^b   Chen, Bailiang ^c   Vuissoz, Pierre André ^c   Gillet, Pierre ^a   Pinzano, Astrid ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UNIVERSITÉ DE LYON   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 2; GAG PROTEIN; NITRIC OXIDE; PROSTAGLANDIN E2; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA1; FERRIC ION; FERRIC OXIDE;

ACAN GENE; ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL LABELING; CELL PROLIFERATION; CELL THERAPY; CELL VIABILITY; CHONDROGENESIS; COL10 GENE; COL2A2 GENE; COMP GENE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; GENE; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; MESENCHYMAL STEM CELL; NON INVASIVE PROCEDURE; NUCLEAR MAGNETIC RESONANCE IMAGING; SOX9 GENE; TISSUE ENGINEERING; TISSUE REGENERATION; BONE MARROW; CARTILAGE; CARTILAGE CELL; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; PROCEDURES; STAINING;

BONE MARROW; CARTILAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE II; FERRIC COMPOUNDS; GENE EXPRESSION; HUMANS; IN VITRO TECHNIQUES; MAGNETIC RESONANCE IMAGING; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; STAINING AND LABELING; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84902310720     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098451     Document Type: Article

References (40)

1. Khan WS, Johnson DS, Hardingham TE (2010) The potential of stem cells in the treatment of knee cartilage defects. Knee 17: 369-374.
2. Pelttari K, Steck E, Richter W (2008) The use of mesenchymal stem cells for chondrogenesis. Injury 39 Suppl 1: S58-65.
3. Hong H, Yang Y, Zhang Y, Cai W (2010) Non-invasive imaging of human embryonic stem cells. Curr Pharm Biotechnol 11: 685-692.
4. Jing XH, Yang L, Duan XJ, Xie B, Chen W, et al. (2008) In vivo MR imaging tracking of magnetic iron oxide nanoparticle labeled, engineered, autologous bone marrow mesenchymal stem cells following intra-articular injection. Joint Bone Spine 75: 432-438.
5. Arbab AS, Jordan EK, Wilson LB, Yocum GT, Lewis BK, et al. (2004) In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum Gene Ther 15: 351-360. (Pubitemid 38469777)
6. Zhu W, Li X, Tang Z, Zhu S, Qi J, et al. (2007) Superparamagnetic iron oxide labeling of neural stem cells and 4.7T MRI tracking in vivo and in vitro. J Huazhong Univ Sci Technolog Med Sci 27: 107-110.
7. Sykova E, Jendelova P, Herynek V (2011) Magnetic resonance imaging of stem cell migration. Methods Mol Biol 750: 79-90.
8. Feng Y, Jin X, Dai G, Liu J, Chen J, et al. (2011) In vitro targeted magnetic delivery and tracking of superparamagnetic iron oxide particles labeled stem cells for articular cartilage defect repair. J Huazhong Univ Sci Technolog Med Sci 31: 204-209.
9. Nieminen MT, Nissi MJ, Mattila L, Kiviranta I (2012) Evaluation of chondral repair using quantitative MRI. J Magn Reson Imaging 36: 1287-1299.
10. Frank JA, Miller BR, Arbab AS, Zywicke HA, Jordan EK, et al. (2003) Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 228: 480-487. (Pubitemid 36910091)
11. Daldrup-Link HE, Rudelius M, Oostendorp RA, Settles M, Piontek G, et al. (2003) Targeting of hematopoietic progenitor cells with MR contrast agents. Radiology 228: 760-767. (Pubitemid 37025487)
12. Schafer R, Kehlbach R, Muller M, Bantleon R, Kluba T, et al. (2009) Labeling of human mesenchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy 11: 68-78.
13. Qi Y, Feng G, Huang Z, Yan W (2013) The application of super paramagnetic iron oxide-labeled mesenchymal stem cells in cell-based therapy. Mol Biol Rep.
14. Farrell E, Wielopolski P, Pavljasevic P, van Tiel S, Jahr H, et al. (2008) Effects of iron oxide incorporation for long term cell tracking on MSC differentiation in vitro and in vivo. Biochem Biophys Res Commun 369: 1076-1081.
15. van Buul GM, Kotek G, Wielopolski PA, Farrell E, Bos PK, et al. (2011) Clinically translatable cell tracking and quantification by MRI in cartilage repair using superparamagnetic iron oxides. PLoS One 6: e17001.
16. Glowacki J, Mizuno S (2008) Collagen scaffolds for tissue engineering. Biopolymers 89: 338-344.
17. Chajra H, Rousseau CF, Cortial D, Ronziere MC, Herbage D, et al. (2008) Collagen-based biomaterials and cartilage engineering. Application to osteochondral defects. Biomed Mater Eng 18: S33-45. (Pubitemid 351366860)
18. Perrier E, Ronziere MC, Bareille R, Pinzano A, Mallein-Gerin F, et al. (2011) Analysis of collagen expression during chondrogenic induction of human bone marrow mesenchymal stem cells. Biotechnol Lett 33: 2091-2101.
19. Henrionnet C, Roeder E, Gillet R, Galois L, Bensoussan D, et al. (2010) Expression of chondrogenic genes by undifferentiated vs. differentiated human mesenchymal stem cells using array technology. Biomed Mater Eng 20: 175-181.
20. Yang CY, Hsiao JK, Tai MF, Chen ST, Cheng HY, et al. (2011) Direct labeling of hMSC with SPIO: the long-term influence on toxicity, chondrogenic differentiation capacity, and intracellular distribution. Mol Imaging Biol 13: 443-451.
21. Boutry S, Brunin S, Mahieu I, Laurent S, Vander Elst L, et al. (2008) Magnetic labeling of non-phagocytic adherent cells with iron oxide nanoparticles: a comprehensive study. Contrast Media Mol Imaging 3: 223-232.
22. Reddy AM, Kwak BK, Shim HJ, Ahn C, Lee HS, et al. (2010) In vivo tracking of mesenchymal stem cells labeled with a novel chitosan-coated super-paramagnetic iron oxide nanoparticles using 3.0T MRI. J Korean Med Sci 25: 211-219.
23. Kostura L, Kraitchman DL, Mackay AM, Pittenger MF, Bulte JW (2004) Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed 17: 513-517. (Pubitemid 39549429)
24. Babic M, Horak D, Trchova M, Jendelova P, Glogarova K, et al. (2008) Poly(L-lysine)-modified iron oxide nanoparticles for stem cell labeling. Bioconjug Chem 19: 740-750. (Pubitemid 351431406)
25. Neri M, Maderna C, Cavazzin C, Deidda-Vigoriti V, Politi LS, et al. (2008) Efficient in vitro labeling of human neural precursor cells with super-paramagnetic iron oxide particles: relevance for in vivo cell tracking. Stem Cells 26: 505-516. (Pubitemid 351413611)
26. Freyria AM, Mallein-Gerin F (2012) Chondrocytes or adult stem cells for cartilage repair: the indisputable role of growth factors. Injury 43: 259-265.
27. Shintani N, Hunziker EB (2011) Differential effects of dexamethasone on the chondrogenesis of mesenchymal stromal cells: influence of microenvironment, tissue origin and growth factor. Eur Cell Mater 22: 302-319; discussion 319-320.
28. Mueller MB, Fischer M, Zellner J, Berner A, Dienstknecht T, et al. (2010) Hypertrophy in mesenchymal stem cell chondrogenesis: effect of TGF-beta isoforms and chondrogenic conditioning. Cells Tissues Organs 192: 158-166.
29. Studer D, Millan C, Ozturk E, Maniura-Weber K, Zenobi-Wong M (2012) Molecular and biophysical mechanisms regulating hypertrophic differentiation in chondrocytes and mesenchymal stem cells. Eur Cell Mater 24: 118-135; discussion 135.
30. Bulte JW, Kraitchman DL, Mackay AM, Pittenger MF (2004) Chondrogenic differentiation of mesenchymal stem cells is inhibited after magnetic labeling with ferumoxides. Blood 104: 3410-3412; author reply 3412-3413.
31. Heymer A, Haddad D, Weber M, Gbureck U, Jakob PM, et al. (2008) Iron oxide labeling of human mesenchymal stem cells in collagen hydrogels for articular cartilage repair. Biomaterials 29: 1473-1483.
32. Boddington SE, Sutton EJ, Henning TD, Nedopil AJ, Sennino B, et al. (2011) Labeling human mesenchymal stem cells with fluorescent contrast agents: the biological impact. Mol Imaging Biol 13: 3-9.
33. Arbab AS, Yocum GT, Rad AM, Khakoo AY, Fellowes V, et al. (2005) Labeling of cells with ferumoxides-protamine sulfate complexes does not inhibit function or differentiation capacity of hematopoietic or mesenchymal stem cells. NMR Biomed 18: 553-559. (Pubitemid 43013896)
34. Farrell E, Wielopolski P, Pavljasevic P, Kops N, Weinans H, et al. (2009) Cell labeling with superparamagnetic iron oxide has no effect on chondrocyte behaviour. Osteoarthritis Cartilage 17: 961-967.
35. Foldager CB, Pedersen M, Ringgaard S, Bunger C, Lind M (2011) Chondrocyte gene expression is affected by very small iron oxide particles-labeling in long-term in vitro MRI tracking. J Magn Reson Imaging 33: 724-730.
36. Saha S, Yang XB, Tanner S, Curran S, Wood D, et al. (2013) The effects of iron oxide incorporation on the chondrogenic potential of three human cell types. J Tissue Eng Regen Med 7: 461-469.
37. Ramaswamy S, Greco JB, Uluer MC, Zhang Z, Zhang Z, et al. (2009) Magnetic resonance imaging of chondrocytes labeled with superparamagnetic iron oxide nanoparticles in tissue-engineered cartilage. Tissue Eng Part A 15: 3899-3910.
38. Chen J, Wang F, Zhang Y, Jin X, Zhang L, et al. (2012) In vivo tracking of superparamagnetic iron oxide nanoparticle labeled chondrocytes in large animal model. Ann Biomed Eng 40: 2568-2578.
39. Terrovitis JV, Bulte JW, Sarvananthan S, Crowe LA, Sarathchandra P, et al. (2006) Magnetic resonance imaging of ferumoxide-labeled mesenchymal stem cells seeded on collagen scaffolds-relevance to tissue engineering. Tissue Eng 12: 2765-2775. (Pubitemid 46141245)
40. Markides H, Kehoe O, Morris RH, El Haj AJ (2013) Whole body tracking of superparamagnetic iron oxide nanoparticle-labeled cells-a rheumatoid arthritis mouse model. Stem Cell Res Ther 4: 126.