Evaluation of ultrasmall superparamagnetic iron oxide contrast agent labeling of equine cord blood and bone marrow mesenchymal stromal cells

American Journal of Veterinary Research

Volumn 75, Issue 11, 2014, Pages 1010-1017

  Bourzac, Celine A ^a,c   Koenig, Judith B ^a   Link, Kaitlyn A ^a   Nykamp, Stephanie G ^a   Koch, Thomas G ^a,b  

^a UNIVERSITY OF GUELPH   (Canada)

^b AARHUS UNIVERSITY   (Denmark)

^c ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIOPEPTIDASE A; FERRIC FERROCYANIDE; ULTRASMALL SUPERPARAMAGNETIC IRON; UNCLASSIFIED DRUG; CONTRAST MEDIUM; DEXTRAN; FERUMOXTRAN-10; MAGNETITE NANOPARTICLE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL LABELING; CELL PROLIFERATION; CELL VIABILITY; CELL VIABILITY ASSAY; CLOSTRIDIUM HISTOLYTICUM; CONTROLLED STUDY; EQUIDAE; FLEXOR TENDON; FLUORESCENCE MICROSCOPY; FORELIMB; HORSE; MICROPHOTOGRAPHY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; STAINING; TENDON LESION; UMBILICAL CORD BLOOD; ANATOMY AND HISTOLOGY; ANIMAL; BLOOD; CADAVER; CYTOLOGY; FEMALE; FETUS BLOOD; MESENCHYMAL STROMA CELL; PLACENTA; PREGNANCY; VETERINARY; VIRUS CULTURE;

ANIMALS; CADAVER; CONTRAST MEDIA; DEXTRANS; FEMALE; FETAL BLOOD; FORELIMB; HORSES; MAGNETIC RESONANCE IMAGING; MAGNETITE NANOPARTICLES; MESENCHYMAL STROMAL CELLS; PLACENTA; PREGNANCY; SERIAL PASSAGE;

EID: 84908283131     PISSN: 00029645     EISSN: 19435681     Source Type: Journal    
DOI: 10.2460/ajvr.75.11.1010     Document Type: Article

References (53)

1. Schnabel LV, Lynch ME, van der Meulen MC, et al. Mesenchy-mal stem cells and insulin-like growth factor-I gene-enhanced mesenchymal stem cells improve structural aspects of healing in equine flexor digitorum superficialis tendons. J Orthop Res 2009;27:1392-1398.
2. Frisbie DD, Kisiday JD, Kawcak CE, et al. Evaluation of adipose-derived stromal vascular fraction or bone marrow-derived mesenchymal stem cells for treatment of osteoarthritis. J Orthop Res 2009;27:1675-1680.
3. Wilke MM, Nydam D V, Nixon AJ. Enhanced early chondro-genesis in articular defects following arthroscopic mesenchy-mal stem cell implantation in an equine model. J Orthop Res 2007;25:913-925.
4. Nixon AJ, Dahlgren LA, Haupt JL, et al. Effect of adipose-derived nucleated cell fractions on tendon repair in horses with collagenase-induced tendinitis. Am J Vet Res 2008;69:928-937.
5. Pacini S, Spinabella S, Trombi L, et al. Suspension of bone marrow-derived undifferentiated mesenchymal stromal cells for repair of superficial digital flexor tendon in race horses. Tissue Eng 2007;13:2949-2955.
6. Smith RK. Mesenchymal stem cell therapy for equine tendinop-athy. Disabil Rehabil 2008;30:1752-1758.
7. Smith RK. Use of bone marrow-derived mesenchymal stem cells to enhance tendon and ligament healing, in Proceedings. Am Coll Vet Surg Vet Symp 2008;172-176
8. Smith RK, Korda M, Blunn G W, et al. Isolation and implantation of autologous equine mesenchymal stem cells from bone marrow into the superficial digital flexor tendon as a potential novel treatment. Equine Vet J 2003;35:99-102.
9. Herthel DJ. Enhanced suspensory ligament healing in 100 horses by stem cells and other bone marrow components, in Proceedings. 47th Am Assoc Equine Pract Annu Conv 2001;319-321.
10. Clegg PD. Biological therapies for treatment of tendon and ligament injuries, in Proceedings. 47th Br Equine Vet Assoc Cong 2008;263-264.
11. Rosenbrock A, Jacobi R, Jaugstetter H, et al. Autologous bone marrow transplantation to stimulate suspensory ligament regeneration in 24 horses-a clinical case control study, in Proceedings. 12th Eur Soc Vet Orthop Traumatol Cong 2004;264-265.
12. Blau HM, Brazelton TR, Weimann JM. The evolving concept of a stem cell: entity or function? Cell 2001;105:829-841.
13. Loeffler M, Roeder I. Tissue stem cells: definition, plasticity, heterogeneity, self-organization and models-a conceptual approach. Cells Tissues Organs 2002;171:8-26.
14. Caplan AI. Why are MSCs therapeutic? New data: new insight. J Pathol 2009;217:318-324.
15. Sole A, Spriet M, Padgett KA, et al. Distribution and persistence of technetium-99 hexamethyl propylene amine oxime-labelled bone marrow-derived mesenchymal stem cells in experimentally induced tendon lesions after intratendinous injection and regional perfusion of the equine distal limb. Equine Vet J 2013;45:726-731.
16. Guest DJ, Smith MR, Allen WR. Monitoring the fate of autolo-gous and allogeneic mesenchymal progenitor cells injected into the superficial digital flexor tendon of horses: preliminary study. Equine Vet J 2008;40:178-181.
17. Drey F, Choi YH, Neef K, et al. Noninvasive in vivo tracking of mesenchymal stem cells and evaluation of cell therapeutic effects in a murine model using a clinical 3.0 T MRI. Cell Transplant 2013;22:1971-1980.
18. Noad J, Gonzalez-Lara LE, Broughton HC, et al. MRI tracking of transplanted iron-labeled mesenchymal stromal cells in an immune-compromised mouse model of critical limb ischemia. NMR Biomed 2013;26:458-467.
19. Yoo JH, Park C, Jung DI, et al. In vivo cell tracking of canine al-logenic mesenchymal stem cells administration via renal arterial catheterization and physiopathological effects on the kidney in two healthy dogs. J Vet Med Sci 2011;73:269-274.
20. Cai J, Zhang X, Wang X, et al. In vivo MR imaging of magnetically labeled mesenchymal stem cells transplanted into rat liver through hepatic arterial injection. Contrast Media Mol Imaging 2008;3:61-66.
21. Arbab AS, Janic B, Knight RA, et al. Detection of migration of locally implanted AC133+ stem cells by cellular magnetic resonance imaging with histological findings. FASEB J 2008;22:3234-3246.
22. Bos C, Delmas Y, Desmouliere A, et al. In vivo MR imaging of in-travascularly injected magnetically labeled mesenchymal stem cells in rat kidney and liver. Radiology 2004;233:781-789.
23. Ittrich H, Lange C, Togel F, et al. In vivo magnetic resonance imaging of iron oxide-labeled, arterially-injected mesenchy-mal stem cells in kidneys of rats with acute ischemic kidney injury: detection and monitoring at 3T. J Magn Reson Imaging 2007;25:1179-1191.
24. Reddy AM, Kwak BK, Shim HJ, et al. In vivo tracking of mesen-chymal stem cells labeled with a novel chitosan-coated super-paramagnetic iron oxide nanoparticles using 3.0T MRI. J Korean Med Sci 2010;25:211-219.
25. Bulte J W. In vivo MRI cell tracking: clinical studies. AJR Am J Roentgenol 2009;193:314-325.
26. Bulte J W, Douglas T, Witwer B, et al. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol 2001;19:1141-1147.
27. Budde MD, Frank JA. Magnetic tagging of therapeutic cells for MRI. J Nucl Med 2009;50:171-174.
28. Jirák D, Kríz J, Herynek V, et al. MRI of transplanted pancreatic islets. Magn Reson Med 2004;52:1228-1233.
29. McFadden C, Mallett CL, Foster PJ. Labeling of multiple cell lines using a new iron oxide agent for cell tracking by MRI. Contrast Media Mol Imaging 2011;6:514-522.
30. Turetschek K, Huber S, Floyd E, et al. MR imaging characterization of microvessels in experimental breast tumors by using a particulate contrast agent with histopathologic correlation. Radiology 2001;218:562-569.
31. Bowen C V, Zhang X, Saab G, et al. Application of the static de-phasing regime theory to superparamagnetic iron-oxide loaded cells. Magn Reson Med 2002;48:52-61.
32. Chen YC, Hsiao JK, Liu HM, et al. The inhibitory effect of super-paramagnetic iron oxide nanoparticle (Ferucarbotran) on osteo-genic differentiation and its signaling mechanism in human mes-enchymal stem cells. Toxicol Appl Pharmacol 2010;245:272-279.
33. Henning TD, Sutton EJ, Kim A, et al. The influence of feru-carbotran on the chondrogenesis of human mesenchymal stem cells. Contrast Media Mol Imaging 2009;4:165-173.
34. Kostura L, Kraitchman DL, Mackay AM, et al. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adi-pogenesis or osteogenesis. NMR Biomed 2004;17:513-517.
35. Farrell E, Wielopolski P, Pavljasevic P, et al. Effects of iron oxide incorporation for long term cell tracking on MSC differentiation in vitro and in vivo. Biochem Biophys Res Commun 2008;369:1076-1081.
36. Berry CC, Wells S, Charles S, et al. Cell response to dextran-derivatised iron oxide nanoparticles post internalisation. Bioma-terials 2004;25:5405-5413.
37. Yang JX, Tang WL, Wang XX. Superparamagnetic iron oxide nanoparticles may affect endothelial progenitor cell migration ability and adhesion capacity. Cytotherapy 2010;12:251-259.
38. Schäfer R, Kehlbach R, Müller M, et al. Labeling of human mes-enchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy 2009;11:68-78.
39. Ren Z, Wang J, Zou C, et al. Labeling of cynomolgus monkey bone marrow-derived mesenchymal stem cells for cell tracking by multimodality imaging. Sci China Life Sci 2011;54:981-987.
40. Addicott B, Willman M, Rodriguez J, et al. Mesenchymal stem cell labeling and in vitro MR characterization at 1.5 T of new SPIO contrast agent: Molday ION Rhodamine-B. Contrast Media Mol Imaging 2011;6:7-18.
41. Groman E V, Bouchard JC, Reinhardt C P, et al. Ultrasmall mixed ferrite colloids as multidimensional magnetic resonance imaging, cell labeling, and cell sorting agents. Bioconjug Chem 2007;18:1763-1771.
42. Vaccaro DE, Yang M, Weinberg JS, et al. Cell tracking using nanoparticles. J Cardiovasc Transl Res 2008;1:217-220.
43. Walczak P, Kedziorek DA, Gilad AA, et al. Applicability and limitations of MR tracking of neural stem cells with asymmetric cell division and rapid turnover: the case of the shiverer dysmy-elinated mouse brain. Magn Reson Med 2007;58:261-269.
44. Sun R, Dittrich J, Le-Huu M, et al. Physical and biological characterization of superparamagnetic iron oxide- and ultrasmall superparamagnetic iron oxide-labeled cells: a comparison. Invest Radiol 2005;40:504-513.
45. Vidal MA, Kilroy GE, Johnson JR, et al. Cell growth characteristics and differentiation frequency of adherent equine bone marrow-derived mesenchymal stromal cells: adipogenic and osteogenic capacity. Vet Surg 2006;35:601-610.
46. Crabbe A, Vandeputte C, Dresselaers T, et al. Effects of MRI contrast agents on the stem cell phenotype. Cell Transplant 2010;19:919-936.
47. Ketkar-Atre A, Struys T, Soenen SJ, et al. Variability in contrast agent uptake by different but similar stem cell types. Int J Nano-medicine 2013;8:4577-4591.
48. Bosch G, Lameris MC, van den Belt AJ, et al. The propagation of induced tendon lesions in the equine superficial digital flexor tendon: an ex vivo study. Equine Vet J 2010;42:407-411.
49. Cox DR, Shell EJ. Analysis of binary data. 2nd ed. London: Chapman & Hall, 1989.
50. Soenen SJ, Himmelreich U, Nuytten N, et al. Intracellular nanoparticle coating stability determines nanoparticle diagnostics efficacy and cell functionality. Small 2010;6:2136-2145.
51. Lévy M, Lagarde F, Maraloiu VA, et al. Degradability of super-paramagnetic nanoparticles in a model of intracellular environment: follow-up of magnetic, structural and chemical properties [published online ahaed of print Sep 6, 2010]. Nanotechnology doi:10.1088/0957-4484/21/39/395103.
52. Frank JA, Anderson SA, Arbab AS. Methods for labeling non-phagocytic cells with MR contrast agents. In: Modo MJ, Bulte J W, eds. Molecular and cellular MR imaging. Boca Raton, Fla: CRC Press, 2007;295-324.
53. Kern S, Eichler H, Stoeve J, et al. Comparative analysis of mes-enchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006;24:1294-1301.