Magnetic resonance imaging of human dental pulp stem cells in vitro and in vivo

Cell Transplantation

Volumn 22, Issue 10, 2013, Pages 1813-1829

  Struys, Tom ^a,b   Ketkar Atre, A ^a   Gervois, P ^b   Leten, C ^a   Hilkens, P ^b   Martens, W ^b   Bronckaers, A ^b   Dresselaers, T ^a   Politis, C ^c   Lambrichts, I ^b   Himmelreich, U ^a  

^a Catholic University of Leuven   (Belgium)

^b HASSELT UNIVERSITY   (Belgium)

^c DEPARTMENT OF CARDIOLOGY   (Belgium)

Author keywords

Cell imaging; Dental pulp; Magnetic resonance imaging (MRI); Mesenchymal stem cells (MSCs); Transmission electron microscopy (TEM)

Indexed keywords

SUPERPARAMAGNETIC IRON OXIDE; TETRAZOLIUM;

ARTICLE; CELL METABOLISM; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; DENTAL PULP STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIMIT OF DETECTION; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; STEM CELL; TOOTH PULP; TRANSMISSION ELECTRON MICROSCOPY;

ADIPOGENESIS; ADOLESCENT; ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; DENTAL PULP; FEMALE; FERROSOFERRIC OXIDE; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETITE NANOPARTICLES; MALE; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; OSTEOGENESIS; POLYLYSINE; STEM CELL TRANSPLANTATION; STEM CELLS; YOUNG ADULT;

EID: 84884682726     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X657774     Document Type: Article

References (54)

1. Aime, S.; Cabella, C.; Colombatto, S.; Geninatti Crich, S.; Gianolio, E.; Maggioni, F. Insights into the use of paramagnetic Gd(III) complexes in MR-molecular imaging investigations. J. Magn. Reson. Imaging 16(4):394-406; 2002.
2. 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 superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 229(3):838-846; 2003.
3. Batouli, S.; Miura, M.; Brahim, J.; Tsutsui, 3. T. W.; Fisher, L. W.; Gronthos, S.; Robey, P. G.; Shi, S. Comparison of stem-cell-mediated osteogenesis and dentinogenesis. J. Dent. Res. 82(12):976-981; 2003.
4. 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. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat. Biotechnol. 19(12): 1141-1147; 2001.
5. Bulte, J. W.; Kraitchman, D. L. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 17(7):484-499; 2004.
6. Caravan, P.; Ellison, J. J.; McMurry, T. J.; Lauffer, R. B. Gadolinium(III) chelates as MRI contrast agents: Structure, dynamics, and applications. Chem. Rev. 99(9):2293-2352; 1999.
7. Chamberlain, G.; Fox, J.; Ashton, B.; Middleton, J. Concise review: Mesenchymal stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25(11):2739-2749; 2007.
8. Collier, A. C.; Pritsos, C. A. The mitochondrial uncoupler dicumarol disrupts the MTT assay. Biochem. Pharmacol. 66(2):281-287; 2003.
9. Crabbe, A.; Vandeputte, C.; Dresselaers, T.; Sacido, A. A.; Verdugo, J. M.; Eyckmans, J.; Luyten, F. P.; Van Laere, K.; Verfaillie, C. M.; Himmelreich, U. Effects of MRI contrast agents on the stem cell phenotype. Cell Transplant. 19(8):919-936; 2010.
10. Dominici, M.; Le Blanc, K.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.; Krause, D.; Deans, R.; Keating, A.; Prockop, D.; Horwitz, E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315-317; 2006.
11. Frank, J. A.; Zywicke, H.; Jordan, E. K.; Mitchell, J.; Lewis, B. K.; Miller, B.; Bryant, Jr., L. H.; Bulte, J. W. Magnetic intracellular labeling of mammalian cells by combining (FDA-approved) superparamagnetic iron oxide MR contrast agents and commonly used transfection agents. Acad. Radiol. 9 Suppl 2:S484-S487; 2002.
12. Giordano, A.; Galderisi, U.; Marino, I. R. From the laboratory bench to the patient's bedside: An update on clinical trials with mesenchymal stem cells. J. Cell. Physiol. 211(1):27-35; 2007.
13. Gronthos, S.; Brahim, J.; Li, W.; Fisher, L. W.; Cherman, N.; Boyde, A.; DenBesten, P.; Robey, P. G.; Shi, S. Stem cell properties of human dental pulp stem cells. J. Dent. Res. 81(8):531-535; 2002.
14. Gronthos, S.; Mankani, M.; Brahim, J.; Robey, P. G.; Shi, S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc. Natl. Acad. Sci. USA 97(25):13625-13630; 2000.
15. Himmelreich, U.; Dresselaers, T. Cell labeling and tracking for experimental models using magnetic resonance imaging. Methods 48(2):112-124; 2009.
16. 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. USA 99(25):16267-16272; 2002.
17. Howard, C.; Murray, P. E.; Namerow, K. N. Dental pulp stem cell migration. J. Endod. 36(12):1963-1966; 2010.
18. Iohara, K.; Zheng, L.; Wake, H.; Ito, M.; Nabekura, J.; Wakita, H.; Nakamura, H.; Into, T.; Matsushita, K.; Nakashima, M. A novel stem cell source for vasculogenesis in ischemia: Subfraction of side population cells from dental pulp. Stem Cells 26(9):2408-2418; 2008.
19. Jendelova, P.; Herynek, V.; Urdzikova, L.; Glogarova, K.; Kroupova, J.; Andersson, B.; Bryja, V.; Burian, M.; Hajek, M.; Sykova, E. Magnetic resonance tracking of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J. Neurosci. Res. 76(2):232-243; 2004.
20. Jones, B. J.; McTaggart, S. J. Immunosuppression by mesenchymal stromal cells: From culture to clinic. Exp. Hematol. 36(6):733-741; 2008.
21. Ju, S.; Teng, G.; Zhang, Y.; Ma, M.; Chen, F.; Ni, Y. In vitro labeling and MRI of mesenchymal stem cells from human umbilical cord blood. Magn. Reson. Imaging 24(5):611-617; 2006.
22. Karussis, D.; Kassis, I. The potential use of stem cells in multiple sclerosis: An overview of the preclinical experience. Clin. Neurol. Neurosurg. 110(9):889-896; 2008.
23. Kerkis, I.; Caplan, A. I. Stem cells in dental pulp of deciduous teeth. Tissue Eng. Part B Rev. 18(2):129-138; 2012.
24. Kidd, S.; Spaeth, E.; Dembinski, J. L.; Dietrich, M.; Watson, K.; Klopp, A.; Battula, V. L.; Weil, M.; Andreeff, M.; Marini, F. C. Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem Cells 27(10):2614-2623; 2009.
25. Kiraly, M.; Kadar, K.; Horvathy, D. B.; Nardai, P.; Racz, G. Z.; Lacza, Z.; Varga, G.; Gerber, G. Integration of neuronally predifferentiated human dental pulp stem cells into rat brain in vivo. Neurochem. Int. 59(3):371-381; 2011.
26. Kustermann, E.; Himmelreich, U.; Kandal, K.; Geelen, T.; Ketkar, A.; Wiedermann, D.; Strecker, C.; Esser, J.; Arnhold, S.; Hoehn, M. Efficient stem cell labeling for MRI studies. Contrast Media Mol. Imaging 3(1):27-37; 2008.
27. Lee, P. H.; Kim, J. W.; Bang, O. Y.; Ahn, Y. H.; Joo, I. S.; Huh, K. Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with multiple system atrophy. Clin. Pharmacol. Ther. 83(5):723-730; 2008.
28. 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(4):410-414; 2000.
29. Lunov, O.; Syrovets, T.; Buchele, B.; Jiang, X.; Rocker, C.; Tron, K.; Nienhaus, G. U.; Walther, P.; Mailander, V.; Landfester, K.; Simmet, T. The effect of carboxydextrancoated superparamagnetic iron oxide nanoparticles on c-Jun N-terminal kinase-mediated apoptosis in human macrophages. Biomaterials 31(19):5063-5071; 2010.
30. Mueller, S. M.; Glowacki, J. Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J. Cell. Biochem. 82(4):583-590; 2001.
31. Nakashima, M.; Iohara, K.; Sugiyama, M. Human dental pulp stem cells with highly angiogenic and neurogenic potential for possible use in pulp regeneration. Cytokine Growth Factor Rev. 20(5-6):435-440; 2009.
32. Nohroudi, K.; Arnhold, S.; Berhorn, T.; Addicks, K.; Hoehn, M.; Himmelreich, U. In vivo MRI stem cell tracking requires balancing of detection limit and cell viability. Cell Transplant. 19(4):431-441; 2010.
33. Omidkhoda, A.; Mozdarani, H.; Movasaghpoor, A.; Fatholah, A. A. Study of apoptosis in labeled mesenchymal stem cells with superparamagnetic iron oxide using neutral comet assay. Toxicol. In Vitro 21(6):1191-1196; 2007.
34. Pittenger, M. F.; Mackay, A. M.; Beck, S. C.; Jaiswal, R. K.; Douglas, R.; Mosca, J. D.; Moorman, M. A.; Simonetti, D. W.; Craig, S.; Marshak, D. R. Multilineage potential of adult human mesenchymal stem cells. Science 284(5411): 143-147; 1999.
35. Rasmusson, I. Immune modulation by mesenchymal stem cells. Exp. Cell Res. 312(12):2169-2179; 2006.
36. Soenen, S. J.; Brisson, A. R.; De Cuyper, M. Addressing the problem of cationic lipid-mediated toxicity: The magnetoliposome model. Biomaterials 30(22):3691-3701; 2009.
37. Soenen, S. J.; Brisson, A. R.; Jonckheere, E.; Nuytten, N.; Tan, S.; Himmelreich, U.; De Cuyper, M. The labeling of cationic iron oxide nanoparticle-resistant hepatocellular carcinoma cells using targeted magnetoliposomes. Biomaterials 32(6):1748-1758; 2011.
38. Soenen, S. J.; Himmelreich, U.; Nuytten, N.; De Cuyper, M. Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials 32(1):195-205; 2011.
39. Soenen, S. J.; Himmelreich, U.; Nuytten, N.; Pisanic, 2nd, T. R.; Ferrari, A.; De Cuyper, M. Intracellular nanoparticle coating stability determines nanoparticle diagnostics efficacy and cell functionality. Small 6(19):2136-2145; 2010.
40. Sordi, V. Mesenchymal stem cell homing capacity. Transplantation 87(9 Suppl.):S42-S45; 2009.
41. Spath, L.; Rotilio, V.; Alessandrini, M.; Gambara, G.; De Angelis, L.; Mancini, M.; Mitsiadis, T. A.; Vivarelli, E.; Naro, F.; Filippini, A.; Papaccio, G. Explant-derived human dental pulp stem cells enhance differentiation and proliferation potentials. J. Cell. Mol. Med. 14(6B):1635-1644; 2010.
42. Stenderup, K.; Justesen, J.; Clausen, C.; Kassem, M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33(6):919-926; 2003.
43. Stroh, A.; Zimmer, C.; Gutzeit, C.; Jakstadt, M.; Marschinke, F.; Jung, T.; Pilgrimm, H.; Grune, T. Iron oxide particles for molecular magnetic resonance imaging cause transient oxidative stress in rat macrophages. Free Radic. Biol. Med. 36(8):976-984; 2004.
44. Struys, T.; Moreels, M.; Martens, W.; Donders, R.; Wolfs, E.; Lambrichts, I. Ultrastructural and immunocytochemical analysis of multilineage differentiated human dental pulpand umbilical cord-derived mesenchymal stem cells. Cells Tissues Organs 193(6):366-378; 2011.
45. Suzuki, T.; Lee, C. H.; Chen, M.; Zhao, W.; Fu, S. Y.; Qi, J. J.; Chotkowski, G.; Eisig, S. B.; Wong, A.; Mao, J. J. Induced migration of dental pulp stem cells for in vivo pulp regeneration. J. Dent. Res. 90(8):1013-1018; 2011.
46. Tyndall, A.; Walker, U. A.; Cope, A.; Dazzi, F.; De Bari, C.; Fibbe, W.; Guiducci, S.; Jones, S.; Jorgensen, C.; Le Blanc, K.; Luyten, F.; McGonagle, D.; Martin, I.; Bocelli-Tyndall, C.; Pennesi, G.; Pistoia, V.; Pitzalis, C.; Uccelli, A.; Wulffraat, N.; Feldmann, M. Immunomodulatory properties of mesenchymal stem cells: A review based on an interdisciplinary meeting held at the Kennedy Institute of Rheumatology Division, London, UK, 31 October 2005. Arthritis Res. Ther. 9(1):301; 2007.
47. Wakitani, S.; Saito, T.; Caplan, A. I. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 18(12):1417-1426; 1995.
48. Wang, X.; Wei, F.; Liu, A.; Wang, L.; Wang, J. C.; Ren, L.; Liu, W.; Tu, Q.; Li, L.; Wang, J. Cancer stem cell labeling using poly(l-lysine)-modified iron oxide nanoparticles. Biomaterials 33(14):3719-3732; 2012.
49. Weissleder, R.; Cheng, H. C.; Bogdanova, A.; Bogdanov, A., Jr. Magnetically labeled cells can be detected by MR imaging. J. Magn. Reson. Imaging 7(1):258-263; 1997.
50. Weissleder, R.; Stark, D. D.; Engelstad, B. L.; Bacon, B. R.; Compton, C. C.; White, D. L.; Jacobs, P.; Lewis, J. Superparamagnetic iron oxide: Pharmacokinetics and toxicity. Am. J. Roentgenol. 152(1):167-173; 1989.
51. Wislet-Gendebien, S.; Hans, G.; Leprince, P.; Rigo, J. M.; Moonen, G.; Rogister, B. Plasticity of cultured mesenchymal stem cells: Switch from nestin-positive to excitable neuron-like phenotype. Stem Cells 23(3):392-402; 2005.
52. Woodbury, D.; Reynolds, K.; Black, I. B. Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J. Neurosci. Res. 69(6):908-917; 2002.
53. Yang, J. X.; Tang, W. L.; Wang, X. X. Superparamagnetic iron oxide nanoparticles may affect endothelial progenitor cell migration ability and adhesion capacity. Cytotherapy 12(2):251-259; 2010.
54. Zhu, M. T.; Wang, Y.; Feng, W. Y.; Wang, B.; Wang, M.; Ouyang, H.; Chai, Z. F. Oxidative stress and apoptosis induced by iron oxide nanoparticles in cultured human umbilical endothelial cells. J. Nanosci. Nanotechnol. 10(12): 8584-8590; 2010.