Magnetic resonance imaging of chondrocytes labeled with superparamagnetic iron oxide nanoparticles in tissue-engineered cartilage

Tissue Engineering - Part A

Volumn 15, Issue 12, 2009, Pages 3899-3910

  Ramaswamy, Sharan ^a   Greco, Jane B ^a   Uluer, Mehmet C ^b   Zhang, Zijun ^b   Zhang, Zhuoli ^a   Fishbein, Kenneth W ^a   Spencer, Richard G ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; CARTILAGE; LABELING; LIGAMENTS; MAGNETIC RESONANCE; MAGNETIC RESONANCE IMAGING; NUCLEIC ACIDS; SUPERPARAMAGNETISM;

CELL LABELING; CHONDROCYTES; CONTRAST AGENT; FOOD AND DRUG ADMINISTRATION; FURTHER DEVELOPMENT; LABELED CELLS; MATRIX; NON DESTRUCTIVE; SPATIAL LOCATION; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLES; SUPERPARAMAGNETIC IRON OXIDES; TISSUE ENGINEERED CARTILAGE; TISSUE-ENGINEERED CONSTRUCTS; TRANSFECTION AGENTS;

IRON OXIDES;

SUPERPARAMAGNETIC IRON OXIDE; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALF (BOVINE); CARTILAGE; CARTILAGE CELL; CARTILAGE MATRIX; CELL LABELING; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG EFFECT; HYDROGEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; TISSUE ENGINEERING;

EID: 72049132637     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0677     Document Type: Article

References (49)

1. Kuo, C.K., Li, W.J., Mauck, R.L., Tuan, R.S. Cartilage tissue engineering: its potential and uses. Curr Opin Rheumatol 18, 64, 2006.
2. Elisseeff, J. Injectable cartilage tissue engineering. Expert Opin Biol Ther 4, 1849, 2004.
3. Neves, A.A., Medcalf, N., Brindle, K. Functional assessment of tissue-engineered meniscal cartilage by magnetic resonance imaging and spectroscopy. Tissue Eng 9, 51, 2003.
4. Novotny, J.E., Turka, C.M., Jeong, C., Wheaton, A.J., Li, C., Presedo, A., Richardson, D.W., Reddy, R., Dodge, G.R. Biomechanical and magnetic resonance characteristics of a cartilage-like equivalent generated in a suspension culture. Tissue Eng 12, 2755, 2006.
5. Trattnig, S., Pinker, K., Krestan, C., Plank, C., Millington, S., Marlovits, S. Matrix-based autologous chondrocyte implan tation for cartilage repair with HyalograftC: two-year follow-up by magnetic resonance imaging. Eur J Radiol 57, 9, 2006.
6. Chawla, K., Klein, T.J., Schumacher, B.L., Jadin, K.D., Shah, B.H., Nakagawa, K., Wong, V.W., Chen, A.C., Masuda, K., Sah, R.L. Short-term retention of labeled chondrocyte sub-populations in stratified tissue-engineered cartilaginous constructs implanted in vivo in mini-pigs. Tissue Eng 13, 1525, 2007.
7. Williams, G.M., Klein, T.J., Sah, R.L. Cell density alters matrix accumulation in two distinct fractions and the mechanical integrity of alginate-chondrocyte constructs. Acta Biomater 1, 625, 2005.
8. Ball, S.T., Goomer, R.S., Ostrander, R.V., Tontz, W.L., Jr., Williams, S.K., Amiel, D. Preincubation of tissue engineered constructs enhances donor cell retention. Clin Orthop Relat Res 420, 276, 2004.
9. Goodstone, N.J., Cartwright, A., Ashton, B. Effects of high molecular weight hyaluronan on chondrocytes cultured within a resorbable gelatin sponge. Tissue Eng 10, 621, 2004.
10. Bulte, J.W., Douglas, T., Witwer, B., Zhang, S.C., Strable, E., Lewis, B.K., Zywicke, H., Miller, B., van Gelderen, P., Moskowitz, B.M., Duncan, I.D., Frank, J.A. Magnetoden-drimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol 19, 1141, 2001.
11. Bulte, J.W., Zhang, S., van Gelderen, P., Herynek, V., Jordan, E.K., Duncan, I.D., Frank, J.A. Neurotransplantation of magnetically labeled oligodendrocyte progenitors: magnetic resonance tracking of cell migration and myelination. Proc Natl Acad Sci U S A 96, 15256, 1999.
12. Dodd, C.H., Hsu, H.C., Chu, W.J., Yang, P., Zhang, H.G., Mountz, J.D., Jr., Zinn, K., Forder, J., Josephson, L., Weis-sleder, R., Mountz, J.M., Mountz, J.D. Normal T-cell response and in vivo magnetic resonance imaging of T cells loaded with HIV transactivator-peptide-derived super-paramagnetic nanoparticles. J Immunol Methods 256, 89, 2001.
13. Frank, J.A., Miller, B.R., Arbab, A.S., Zywicke, H.A., Jordan, E.K., Lewis, B.K., Bryant, L.H., Jr., Bulte, J.W. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 228, 480, 2003.
14. Josephson, L., Tung, C.H., Moore, A., Weissleder, R. High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. Bioconjug Chem 10, 186, 1999.
15. Lewin, M., Carlesso, N., Tung, C.H., Tang, X.W., Cory, D., Scadden, D.T., Weissleder, R. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat Biotechnol 18, 410, 2000.
16. Wang, L., Deng, J., Wang, J., Xiang, B., Yang, T., Gruwel, M., Kashour, T., Tomanek, B., Summer, R., Freed, D., Jassal, D.S., Dai, G., Glogowski, M., Deslauriers, R., Arora, R.C., Tian, G. Superparamagnetic iron oxide does not affect the viability and function of adipose-derived stem cells, and superparamagnetic iron oxide-enhanced magnetic resonance imaging identifies viable cells. Magn Reson Imaging 27, 108, 2009.
17. Farrell, E., Wielopolski, P., Pavljasevic, P., van Tiel, S., Jahr, H., Verhaar, J., Weinans, H., Krestin, G., O'Brien, F.J., van Osch, G., Bernsen, M. Effects of iron oxide incorporation for long term cell tracking on MSC differentiation in vitro and in vivo. Biochem Biophys Res Commun 369, 1076, 2008.
18. Chen, C.T., Fishbein, K.W., Torzilli, P.A., Hilger, A., Spencer, R.G., Horton, W.E., Jr. Matrix fixed-charge density as determined by magnetic resonance microscopy of bioreactor-derived hyaline cartilage correlates with biochemical and biomechanical properties. Arthritis Rheum 48, 1047, 2003.
19. Petersen, E.F., Fishbein, K.W., McFarland, E.W., Spencer, R.G. 31P NMR spectroscopy of developing cartilage produced from chick chondrocytes in a hollow-fiber bioreactor. Magn Reson Med 44, 367, 2000.
20. Potter, K., Butler, J.J., Adams, C., Fishbein, K.W., McFarland, E.W., Horton, W.E., Spencer, R.G. Cartilage formation in a hollow fiber bioreactor studied by proton magnetic resonance microscopy. Matrix Biol 17, 513, 1998.
21. Anseth, K.S., Metters, A.T., Bryant, S.J., Martens, P.J., Elis-seeff, J.H., Bowman, C.N. In situ forming degradable networks and their application in tissue engineering and drug delivery. J Control Release 78, 199, 2002.
22. Elisseeff, J., McIntosh, W., Anseth, K., Riley, S., Ragan, P., Langer, R. Photoencapsulation of chondrocytes in poly(eth-ylene oxide)-based semi-interpenetrating networks. J Biomed Mater Res 51, 164, 2000.
23. Wang, D.A., Williams, C.G., Li, Q., Sharma, B., Elisseeff, J.H. Synthesis and characterization of a novel degradable phosphate-containing hydrogel. Biomaterials 24, 3969, 2003.
24. Arbab, A.S., Bashaw, L.A., Miller, B.R., Jordan, E.K., Lewis, B.K., Kalish, H., Frank, J.A. Characterization of biophysical and metabolic properties of cells labeled with super-paramagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 229, 838, 2003.
25. Zhang, Z., van den Bos, E.J., Wielopolski, P.A., de Jong-Popijus, M., Duncker, D.J., Krestin, G.P. High-resolution magnetic resonance imaging of iron-labeled myoblasts using a standard 1.5-T clinical scanner. MAGMA 17, 201, 2004.
26. Potter, K., Butler, J.J., Horton, W.E., Spencer, R.G. Response of engineered cartilage tissue to biochemical agents as studied by proton magnetic resonance microscopy. Arthritis Rheum 43, 1580, 2000.
27. Farndale, R.W., Buttle, D.J., Barrett, A.J. Improved quanti-tation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883, 173, 1986.
28. Anderson, S.A., Shukaliak-Quandt, J., Jordan, E.K., Arbab, A.S., Martin, R., McFarland, H., Frank, J.A. Magnetic resonance imaging of labeled T-cells in a mouse model of multiple sclerosis. Ann Neurol 55, 654, 2004.
29. Arbab, A.S., Yocum, G.T., Rad, A.M., Khakoo, A.Y., Fel-lowes, V., Read, E.J., Frank, J.A. 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, 2005.
30. Daldrup-Link, H.E., Rudelius, M., Oostendorp, R.A., Settles, M., Piontek, G., Metz, S., Rosenbrock, H., Keller, U., Heinzmann, U., Rummeny, E.J., Schlegel, J., Link, T.M. Targeting of hematopoietic progenitor cells with MR contrast agents. Radiology 228, 760, 2003.
31. Hill, J.M., Dick, A.J., Raman, V.K., Thompson, R.B., Yu, Z.X., Hinds, K.A., Pessanha, B.S., Guttman, M.A., Varney, T.R., Martin, B.J., Dunbar, C.E., McVeigh, E.R., Lederman, R.J. Serial cardiac magnetic resonance imaging of injected mes-enchymal stem cells. Circulation 108, 1009, 2003.
32. Hoehn, M., Kustermann, E., Blunk, J., Wiedermann, D., Trapp, T., Wecker, S., Focking, M., Arnold, H., Hescheler, J., Fleischmann, B.K., Schwindt, W., Buhrle, C. Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci U S A 99, 16267, 2002.
33. Kircher, M.F., Allport, J.R., Graves, E.E., Love, V., Josephson, L., Lichtman, A.H., Weissleder, R. In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors. Cancer Research 63, 6838, 2003.
34. Kraitchman, D.L., Heldman, A.W., Atalar, E., Amado, L.C., Martin, B.J., Pittenger, M.F., Hare, J.M., Bulte, J.W. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 107, 2290, 2003.
35. Moore, A., Sun, P.Z., Cory, D., Hogemann, D., Weissleder, R., Lipes, M.A. MRI of insulitis in autoimmune diabetes. Magn Reson Med 47, 751, 2002.
36. Terrovitis, J.V., Bulte, J.W., Sarvananthan, S., Crowe, L.A., Sarathchandra, P., Batten, P., Sachlos, E., Chester, A.H., Czernuszka, J.T., Firmin, D.N., Taylor, P.M., Yacoub, M.H. Magnetic resonance imaging of ferumoxide-labeled mesen-chymal stem cells seeded on collagen scaffolds-relevance to tissue engineering. Tissue Eng 12, 2765, 2006.
37. Ko, I.K., Song, H.T., Cho, E.J., Lee, E.S., Huh, Y.M., Suh, J.S. In vivo MR imaging of tissue-engineered human mesen-chymal stem cells transplanted to mouse: a preliminary study. Ann Biomed Eng 35, 101, 2007.
38. Frangioni, J.V., Hajjar, R.J. In vivo tracking of stem cells for clinical trials in cardiovascular disease. Circulation 110, 3378, 2004.
39. Jobanputra, P., Parry, D., Fry-Smith, A., Burls, A. Effectiveness of autologous chondrocyte transplantation for hyaline cartilage defects in knees: a rapid and systematic review. Health Technol Assess 5, 1, 2001.
40. Minas, T., Peterson, L. Advanced techniques in autologous chondrocyte transplantation. Clin Sports Med 18, 13, 1999.
41. Peterson, L., Minas, T., Brittberg, M., Nilsson, A., Sjogren-Jansson, E., Lindahl, A. Two-to 9-year outcome after autologous chondrocyte transplantation of the knee. Clin Orthop Relat Res 374, 212, 2000.
42. Ronga, M., Grassi, F.A., Bulgheroni, P. Arthroscopic autol-ogous chondrocyte implantation for the treatment of a chondral defect in the tibial plateau of the knee. Arthroscopy 20, 79, 2004.
43. Trippel, S.B. Autologous chondrocyte transplantation. N Engl J Med 332, 539, 1995.
44. Heymer, A., Haddad, D., Weber, M., Gbureck, U., Jakob, P.M., Eulert, J., Noth, U. Iron oxide labelling of human mesenchymal stem cells in collagen hydrogels for articular cartilage repair. Biomaterials 29, 1473, 2008.
45. Farrell, E., Wielopolski, P., Pavljasevic, P., Kops, N., Wei-nans, H., Bernsen, M.R., van Osch, G.J. Cell labelling with superparamagnetic iron oxide has no effect on chondrocyte behaviour. Osteoarthritis Cartilage 17, 958, 2009.
46. Akens, M.K., Hurtig, M.B. Influence of species and anatomical location on chondrocyte expansion. BMC Muscu-loskelet Disord 6, 23, 2005.
47. Greco, J.B., Spencer, R.G. Cartilage growth in magnetic resonance microscopy-compatible hollow fiber bioreactors. In: Chaudhuri, J., Al-Rubeai, M., eds. Bioreactors for Tissue Engineering: Principles, Design and Operation. Dordrecht, The Netherlands: Springer Publishers, 2005, pp. 135-163.
48. Bulte, J.W., Kraitchman, D.L., Mackay, A.M., Pittenger, M.F. Chondrogenic differentiation of mesenchymal stem cells is inhibited after magnetic labeling with ferumoxides. Blood 104, 3410, 2004.
49. Kostura, L., Kraitchman, D.L., Mackay, A.M., Pittenger, M.F., Bulte, J.W. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed 17, 513, 2004.