Skip to main content
SpringerLink
Log in

Stem Cell Tracing Through MR Molecular Imaging

  • Review Article
  • Published:
Tissue Engineering and Regenerative Medicine Aims and scope

Abstract

Stem cell therapy opens a new window in medicine to overcome several diseases that remain incurable. It appears such diseases as cardiovascular disorders, brain injury, multiple sclerosis, urinary system diseases, cartilage lesions and diabetes are curable with stem cell transplantation. However, some questions related to stem cell therapy have remained unanswered. Stem cell imaging allows approval of appropriated strategies such as selection of the type and dose of stem cell, and also mode of cell delivery before being tested in clinical trials. MRI as a non-invasive imaging modality provides proper conditions for this aim. So far, different contrast agents such as superparamagnetic or paramagnetic nanoparticles, ultrasmall superparamagnetic nanoparticles, fluorine, gadolinium and some types of reporter genes have been used for imaging of stem cells. The core subject of these studies is to investigate the survival and differentiation of stem cells, contrast agent’s toxicity and long term following of transplanted cells. The promising results of in vivo and some clinical trial studies may raise hope for clinical stem cells imaging with MRI.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Adopted from Cromer Berman et al. [103], with permission

Similar content being viewed by others

References

  1. Ikehara S. Grand challenges in stem cell treatments. Front Cell Dev Biol. 2013;1:2.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Choumerianou DM, Dimitriou H, Kalmanti M. Stem cells: promises versus limitations. Tissue Eng Part B Rev. 2008;14:53–60.

    Article  PubMed  CAS  Google Scholar 

  3. Lodi D, Iannitti T, Palmieri B. Stem cells in clinical practice: applications and warnings. J Exp Clin Cancer Res. 2011;30:9.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mahla RS. Stem cells applications in regenerative medicine and disease therapeutics. Int J Cell Biol. 2016;2016:6940283.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Abdi R, Fiorina P, Adra CN, Atkinson M, Sayegh MH. Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes. Diabetes. 2008;57:1759–67.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. 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. 2007;25:2739–49.

    Article  PubMed  CAS  Google Scholar 

  7. Ankrum J, Karp JM. Mesenchymal stem cell therapy: Two steps forward, one step back. Trends Mol Med. 2010;16:203–9.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Volarevic V, Erceg S, Bhattacharya SS, Stojkovic P, Horner P, Stojkovic M. Stem cell-based therapy for spinal cord injury. Cell Transplant. 2013;22:1309–23.

    Article  PubMed  Google Scholar 

  9. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, Summers R, et al. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A. 2005;102:14069–74.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Salazar DL, Uchida N, Hamers FP, Cummings BJ, Anderson AJ. Human neural stem cells differentiate and promote locomotor recovery in an early chronic spinal cord injury NOD-scid mouse model. PLoS One. 2010;5:e12272.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Wobus AM, Boheler KR. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev. 2005;85:635–78.

    Article  PubMed  CAS  Google Scholar 

  12. Trounson A, McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell. 2015;17:11–22.

    Article  PubMed  CAS  Google Scholar 

  13. Spiriev T, Sandu N, Schaller B. Molecular imaging and tracking stem cells in neurosciences. Methods Mol Biol. 2013;1052:195–201.

    Article  PubMed  CAS  Google Scholar 

  14. Sandu N, Momen-Heravi F, Sadr-Eshkevari P, Schaller B. Molecular imaging for stem cell transplantation in neuroregenerative medicine. Neurodegener Dis. 2012;9:60–7.

    Article  PubMed  CAS  Google Scholar 

  15. McColgan P, Sharma P, Bentley P. Stem cell tracking in human trials: a meta-regression. Stem Cell Rev. 2011;7:1031–40.

    Article  PubMed  Google Scholar 

  16. Guzman R, Uchida N, Bliss TM, He D, Christopherson KK, Stellwagen D, et al. Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc Natl Acad Sci U S A. 2007;104:10211–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Nguyen PK, Riegler J, Wu JC. Stem cell imaging: from bench to bedside. Cell Stem Cell. 2014;14:431–44.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Srivastava AK, Kadayakkara DK, Bar-Shir A, Gilad AA, McMahon MT, Bulte JW. Advances in using MRI probes and sensors for in vivo cell tracking as applied to regenerative medicine. Dis Model Mech. 2015;8:323–36.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Ngen EJ, Artemov D. Advances in monitoring cell-based therapies with magnetic resonance imaging: future perspectives. Int J Mol Sci. 2017;18:E198.

    Article  PubMed  Google Scholar 

  20. Saito S, Tsugeno M, Koto D, Mori Y, Yoshioka Y, Nohara S, et al. Impact of surface coating and particle size on the uptake of small and ultrasmall superparamagnetic iron oxide nanoparticles by macrophages. Int J Nanomedicine. 2012;7:5415–21.

    PubMed  PubMed Central  CAS  Google Scholar 

  21. Muja N, Bulte JW. Magnetic resonance imaging of cells in experimental disease models. Prog Nucl Magn Reson Spectrosc. 2009;55:61–77.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Jin R, Lin B, Li D, Ai H. Superparamagnetic iron oxide nanoparticles for MR imaging and therapy: design considerations and clinical applications. Curr Opin Pharmacol. 2014;18:18–27.

    Article  PubMed  CAS  Google Scholar 

  23. Gutteridge JM, Rowley DA, Halliwell B. Superoxide-dependent formation of hydroxyl radicals and lipid peroxidation in the presence of iron salts. Detection of ‘catalytic’ iron and anti-oxidant activity in extracellular fluids. Biochem J. 1982;206:605–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Emerit J, Beaumont C, Trivin F. Iron metabolism, free radicals, and oxidative injury. Biomed Pharmacother. 2001;55:333–9.

    Article  PubMed  CAS  Google Scholar 

  25. Barrow M, Taylor A, Murray P, Rosseinsky MJ, Adams DJ. Design considerations for the synthesis of polymer coated iron oxide nanoparticles for stem cell labelling and tracking using MRI. Chem Soc Rev. 2015;44:6733–48.

    Article  PubMed  CAS  Google Scholar 

  26. Lee NK, Kim HS, Yoo D, Hwang JW, Choi SJ, Oh W, et al. Magnetic resonance imaging of ferumoxytol-labeled human mesenchymal stem cells in the mouse brain. Stem Cell Rev. 2017;13:127–38.

    Article  PubMed  CAS  Google Scholar 

  27. Brewer KD, Spitler R, Lee KR, Chan AC, Barrozo JC, Wakeel A, et al. Characterization of magneto-endosymbionts as MRI cell labeling and tracking agents. Mol Imaging Biol. 2017. https://doi.org/10.1007/s11307-017-1093-7.

    Article  Google Scholar 

  28. Lee S, Yoon HI, Na JH, Jeon S, Lim S, Koo H, et al. In vivo stem cell tracking with imageable nanoparticles that bind bioorthogonal chemical receptors on the stem cell surface. Biomaterials. 2017;139:12–29.

    Article  PubMed  CAS  Google Scholar 

  29. Liu L, Ho C. Mesenchymal Stem Cell Preparation and Transfection-free Ferumoxytol Labeling for MRI Cell Tracking. Curr Protoc Stem Cell Biol. 2017;43:2B.7.1–14.

    Article  Google Scholar 

  30. Khurana A, Nejadnik H, Chapelin F, Lenkov O, Gawande R, Lee S, et al. Ferumoxytol: a new, clinically applicable label for stem-cell tracking in arthritic joints with MRI. Nanomedicine (Lond). 2013;8:1969–83.

    Article  CAS  Google Scholar 

  31. Muthiah M, Park IK, Cho CS. Surface modification of iron oxide nanoparticles by biocompatible polymers for tissue imaging and targeting. Biotechnol Adv. 2013;31:1224–36.

    Article  PubMed  CAS  Google Scholar 

  32. Wang YX, Xuan S, Port M, Idee JM. Recent advances in superparamagnetic iron oxide nanoparticles for cellular imaging and targeted therapy research. Curr Pharm Des. 2013;19:6575–93.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Shapiro EM, Sharer K, Skrtic S, Koretsky AP. In vivo detection of single cells by MRI. Magn Reson Med. 2006;55:242–9.

    Article  PubMed  Google Scholar 

  34. Heyn C, Bowen CV, Rutt BK, Foster PJ. Detection threshold of single SPIO-labeled cells with FIESTA. Magn Reson Med. 2005;53:312–20.

    Article  PubMed  Google Scholar 

  35. Bulte JW, Duncan ID, Frank JA. In vivo magnetic resonance tracking of magnetically labeled cells after transplantation. J Cereb Blood Flow Metab. 2002;22:899–907.

    Article  PubMed  Google Scholar 

  36. Di Marco M, Sadun C, Port M, Guilbert I, Couvreur P, Dubernet C. Physicochemical characterization of ultrasmall superparamagnetic iron oxide particles (USPIO) for biomedical application as MRI contrast agents. Int J Nanomedicine. 2007;2:609–22.

    PubMed  PubMed Central  CAS  Google Scholar 

  37. Zhao X, Zhao H, Chen Z, Lan M. Ultrasmall superparamagnetic iron oxide nanoparticles for magnetic resonance imaging contrast agent. J Nanosci Nanotechnol. 2014;14:210–20.

    Article  PubMed  CAS  Google Scholar 

  38. Ariza de Schellenberger A, Kratz H, Farr TD, Löwa N, Hauptmann R, Wagner S, et al. Labeling of mesenchymal stem cells for MRI with single-cell sensitivity. Int J Nanomedicine. 2016;11:1517–35.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Morawski AM, Winter PM, Yu X, Fuhrhop RW, Scott MJ, Hockett F, et al. Quantitative “magnetic resonance immunohistochemistry” with ligand-targeted 19F nanoparticles. Magn Reson Med. 2004;52:1255–62.

    Article  PubMed  CAS  Google Scholar 

  40. Ahrens ET, Zhong J. In vivo MRI cell tracking using perfluorocarbon probes and fluorine-19 detection. NMR Biomed. 2013;26:860–71.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Gaudet JM, Ribot EJ, Chen Y, Gilbert KM, Foster PJ. Tracking the fate of stem cell implants with fluorine-19 MRI. PLoS One. 2015;10:e0118544.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Ahrens ET, Helfer BM, O’Hanlon CF, Schirda C. Clinical cell therapy imaging using a perfluorocarbon tracer and fluorine-19 MRI. Magn Reson Med. 2014;72:1696–701.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Zhong J, Mills PH, Hitchens TK, Ahrens ET. Accelerated fluorine-19 MRI cell tracking using compressed sensing. Magn Reson Med. 2013;69:1683–90.

    Article  PubMed  CAS  Google Scholar 

  44. Gaudet JM, Hamilton AM, Chen Y, Fox MS, Foster PJ. Application of dual 19F and iron cellular MRI agents to track the infiltration of immune cells to the site of a rejected stem cell transplant. Magn Reson Med. 2017;78:713–20.

    Article  PubMed  CAS  Google Scholar 

  45. Tseng CL, Shih IL, Stobinski L, Lin FH. Gadolinium hexanedione nanoparticles for stem cell labeling and tracking via magnetic resonance imaging. Biomaterials. 2010;31:5427–35.

    Article  PubMed  CAS  Google Scholar 

  46. Ludemann L, Wurm R, Zimmer C. Pharmacokinetic modeling of Gd-DTPA extravasation in brain tumors. Investig Radiol. 2002;37:562–70.

    Article  Google Scholar 

  47. Ngen EJ, Wang L, Kato Y, Krishnamachary B, Zhu W, Gandhi N, et al. Imaging transplanted stem cells in real time using an MRI dual-contrast method. Sci Rep. 2015;5:13628.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Liu Y, He ZJ, Xu B, Wu QZ, Liu G, Zhu H, et al. Evaluation of cell tracking effects for transplanted mesenchymal stem cells with jetPEI/Gd-DTPA complexes in animal models of hemorrhagic spinal cord injury. Brain Res. 2011;1391:24–35.

    Article  PubMed  CAS  Google Scholar 

  49. Guenoun J, Koning GA, Doeswijk G, Bosman L, Wielopolski PA, Krestin GP, et al. Cationic Gd-DTPA liposomes for highly efficient labeling of mesenchymal stem cells and cell tracking with MRI. Cell Transplant. 2012;21:191–205.

    Article  PubMed  Google Scholar 

  50. Shen J, Cheng LN, Zhong XM, Duan XH, Guo RM, Hong GB. Efficient in vitro labeling rabbit neural stem cell with paramagnetic Gd-DTPA and fluorescent substance. Eur J Radiol. 2010;75:397–405.

    Article  PubMed  Google Scholar 

  51. Xiao Y, Liu Y, Yang S, Zhang B, Wang T, Jiang D, et al. Sorafenib and gadolinium co-loaded liposomes for drug delivery and MRI-guided HCC treatment. Colloids Surf B Biointerfaces. 2016;141:83–92.

    Article  PubMed  CAS  Google Scholar 

  52. Guo C, Sun L, She W, Li N, Jiang L, Luo K, et al. A dendronized heparin–gadolinium polymer self-assembled into a nanoscale system as a potential magnetic resonance imaging contrast agent. Polym Chem. 2016;7:2531–41.

    Article  CAS  Google Scholar 

  53. Murphy SV, Hale A, Reid T, Olson J, Kidiyoor A, Tan J, et al. Use of trimetasphere metallofullerene MRI contrast agent for the non-invasive longitudinal tracking of stem cells in the lung. Methods. 2016;99:99–111.

    Article  PubMed  CAS  Google Scholar 

  54. Gilad AA, Winnard PT Jr, van Zijl PC, Bulte JW. Developing MR reporter genes: promises and pitfalls. NMR Biomed. 2007;20:275–90.

    Article  PubMed  CAS  Google Scholar 

  55. Vandsburger MH, Radoul M, Cohen B, Neeman M. MRI reporter genes: applications for imaging of cell survival, proliferation, migration and differentiation. NMR Biomed. 2013;26:872–84.

    Article  PubMed  CAS  Google Scholar 

  56. Sherry AD, Woods M. Chemical exchange saturation transfer contrast agents for magnetic resonance imaging. Annu Rev Biomed Eng. 2008;10:391–411.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Vande Velde G, Himmelreich U, Neeman M. Reporter gene approaches for mapping cell fate decisions by MRI: promises and pitfalls. Contrast Media Mol Imaging. 2013;8:424–31.

    Article  PubMed  CAS  Google Scholar 

  58. Kraitchman DL, Bulte JW. Imaging of stem cells using MRI. Basic Res Cardiol. 2008;103:105–13.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Pereira SM, Moss D, Williams SR, Murray P, Taylor A. Overexpression of the MRI reporter genes ferritin and transferrin receptor affect iron homeostasis and produce limited contrast in mesenchymal stem cells. Int J Mol Sci. 2015;16:15481–96.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Deans AE, Wadghiri YZ, Bernas LM, Yu X, Rutt BK, Turnbull DH. Cellular MRI contrast via coexpression of transferrin receptor and ferritin. Magn Reson Med. 2006;56:51–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Patrick PS, Rodrigues TB, Kettunen MI, Lyons SK, Neves AA, Brindle KM. Development of Timd2 as a reporter gene for MRI. Patrick PS, Rodrigues TB, Kettunen. 2016;75:1697–707.

    CAS  Google Scholar 

  62. Dai HY, He R, Zhang Y, Wu RH, Xiao YY. Adenoviral vector mediated ferritin over-expression in mesenchymal stem cells detected by 7T MRI in vitro. PLoS One. 2017;12:e0185260.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Brewer KD, Spitler R, Lee KR, Chan AC, Barrozo JC, Wakeel A, et al. Characterization of magneto-endosymbionts as MRI cell labeling and tracking agents. Mol Imaging Biol. 2017. https://doi.org/10.1007/s11307-017-1093-7.

    Article  Google Scholar 

  64. Guo R, Li Q, Yang F, Hu X, Jiao J, Guo Y, et al. In vivo MR imaging of dual MRI reporter genes and Deltex-1 gene-modified human mesenchymal stem cells in the treatment of closed penile fracture. Mol Imaging Biol. 2017. https://doi.org/10.1007/s11307-017-1128-0.

    Article  Google Scholar 

  65. Liu M, Wang Y, Li M, Zhang Y, Lan X. Using the tyrosinase gene as a tri-modality reporter gene for monitoring transplanted stem cells in acute myocardial infarction. J Nucl Med. 2017;58:167.

    Google Scholar 

  66. Wu MR, Liu HM, Lu CW, Shen WH, Lin IJ, Liao LW, et al. Organic anion-transporting polypeptide 1B3 as a dual reporter gene for fluorescence and magnetic resonance imaging. FASEB J. 2017. https://doi.org/10.1096/fj.201700767R.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Reddy KS, Yusuf S. Emerging epidemic of cardiovascular disease in developing countries. Circulation. 1998;97:596–601.

    Article  PubMed  CAS  Google Scholar 

  68. Kraitchman DL, Heldman AW, Atalar E, Amado LC, Martin BJ, Pittenger MF, et al. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation. 2003;107:2290–3.

    Article  PubMed  Google Scholar 

  69. Hua P, Wang YY, Liu LB, Liu JL, Liu JY, Yang YQ, et al. In vivo magnetic resonance imaging tracking of transplanted superparamagnetic iron oxide-labeled bone marrow mesenchymal stem cells in rats with myocardial infarction. Mol Med Rep. 2015;11:113–20.

    Article  PubMed  CAS  Google Scholar 

  70. Kim YJ, Huh YM, Choe KO, Choi BW, Choi EJ, Jang Y, et al. In vivo magnetic resonance imaging of injected mesenchymal stem cells in rat myocardial infarction; simultaneous cell tracking and left ventricular function measurement. Int J Cardiovasc Imaging. 2009;25:99–109.

    Article  PubMed  CAS  Google Scholar 

  71. Li SH, Lai TY, Sun Z, Han M, Moriyama E, Wilson B, et al. Tracking cardiac engraftment and distribution of implanted bone marrow cells: comparing intra-aortic, intravenous, and intramyocardial delivery. J Thorac Cardiovasc Surg. 2009;137:1225–33.

    Article  PubMed  Google Scholar 

  72. Campan M, Lionetti V, Aquaro GD, Forini F, Matteucci M, Vannucci L, et al. Ferritin as a reporter gene for in vivo tracking of stem cells by 1.5-T cardiac MRI in a rat model of myocardial infarction. Am J Physiol Heart Circ Physiol. 2011;300:H2238–50.

    Article  PubMed  CAS  Google Scholar 

  73. He G, Zhang H, Wei H, Wang Y, Zhang X, Tang Y, et al. In vivo imaging of bone marrow mesenchymal stem cells transplanted into myocardium using magnetic resonance imaging: a novel method to trace the transplanted cells. Int J Cardiol. 2007;114:4–10.

    Article  PubMed  Google Scholar 

  74. Sumino Y, Mimata H. Regenerative medicine as a new therapeutic strategy for lower urinary tract dysfunction. Int J Urol. 2013;20:670–5.

    Article  PubMed  Google Scholar 

  75. Lin CS. Advances in stem cell therapy for the lower urinary tract. World J Stem Cells. 2010;2:1–4.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Adamowicz J, Kloskowski T, Tworkiewicz J, Pokrywczyńska M, Drewa T. Urine is a highly cytotoxic agent: does it influence stem cell therapies in urology? Transplant Proc. 2012;44:1439–41.

    Article  PubMed  CAS  Google Scholar 

  77. Song YS, Ku JH. Monitoring transplanted human mesenchymal stem cells in rat and rabbit bladders using molecular magnetic resonance imaging. Neurourol Urodyn. 2007;26:584–93.

    Article  PubMed  Google Scholar 

  78. Lee HJ, Won JH, Doo SH, Kim JH, Song KY, Lee SJ, et al. Inhibition of collagen deposit in obstructed rat bladder outlet by transplantation of superparamagnetic iron oxide-labeled human mesenchymal stem cells as monitored by molecular magnetic resonance imaging (MRI). Cell Transplant. 2012;21:959–70.

    Article  PubMed  Google Scholar 

  79. Lee HJ, Doo SW, Kim DH, Cha YJ, Kim JH, Song YS, et al. Cytosine deaminase-expressing human neural stem cells inhibit tumor growth in prostate cancer-bearing mice. Cancer Lett. 2013;335:58–65.

    Article  PubMed  CAS  Google Scholar 

  80. Rivière C, Lecoeur C, Wilhelm C, Péchoux C, Combrisson H, Yiou R, et al. The MRI assessment of intraurethrally—delivered muscle precursor cells using anionic magnetic nanoparticles. Biomaterials. 2009;30:6920–8.

    Article  PubMed  Google Scholar 

  81. Song YS, Ku JH, Song ES, Kim JH, Jeon JS, Lee KH, et al. Magnetic resonance evaluation of human mesenchymal stem cells in corpus cavernosa of rats and rabbits. Asian J Androl. 2007;9:361–7.

    Article  PubMed  CAS  Google Scholar 

  82. Aghayan HR, Soleimani M, Goodarzi P, Norouzi-Javidan A, Emami-Razavi SH, Larijani B, et al. Magnetic resonance imaging of transplanted stem cell fate in stroke. J Res Med Sci. 2014;19:465–71.

    PubMed  PubMed Central  Google Scholar 

  83. Jendelová P, Herynek V, Urdzikova L, Glogarová K, Kroupová J, Andersson B, et al. 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. 2004;76:232–43.

    Article  PubMed  Google Scholar 

  84. Syková E, Jendelová P. Magnetic resonance tracking of transplanted stem cells in rat brain and spinal cord. Neurodegener Dis. 2006;3:62–7.

    Article  PubMed  Google Scholar 

  85. Lindvall O, Kokaia Z, Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders—how to make it work. Nat Med. 2004;10:S42–50.

    Article  PubMed  Google Scholar 

  86. Sugaya K. Potential use of stem cells in neuroreplacement therapies for neurodegenerative diseases. Int Rev Cytol. 2003;228:1–30.

    Article  PubMed  Google Scholar 

  87. Sykova E, Jendelova P. In vivo tracking of stem cells in brain and spinal cord injury. Prog Brain Res. 2007;161:367–83.

    Article  PubMed  CAS  Google Scholar 

  88. Zhao JY, Chen G, Gu YP, Cui R, Zhang ZL, Yu ZL, et al. Ultrasmall magnetically engineered Ag2Se quantum dots for instant efficient labeling and whole-body high-resolution multimodal real-time tracking of cell-derived microvesicles. J Am Chem Soc. 2016;138:1893–903.

    Article  PubMed  CAS  Google Scholar 

  89. Kubo T, Baba T, Ikezaki K, Sekiguchi H, Nishino Y, Miyazawa A, et al. Realtime single molecular motion analysis of nicotinic acetylcholine receptor Alpha 7 by diffracted X-Ray tracking method. Biophys J. 2016;110:222a.

    Article  Google Scholar 

  90. Odeleye AOO, Castillo-Avila S, Boon M, Martin H, Coopman K. Development of an optical system for the non-invasive tracking of stem cell growth on microcarriers. Biotechnol Bioeng. 2017;114:2032–42.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Walczak P, Wojtkiewicz J, Nowakowski A, Habich A, Holak P, Xu J, et al. Real-time MRI for precise and predictable intra-arterial stem cell delivery to the central nervous system. J Cereb Blood Flow Metab. 2017;37:2346–58.

    Article  PubMed  Google Scholar 

  92. Zhu J, Zhou L, XingWu F. Tracking neural stem cells in patients with brain trauma. N Engl J Med. 2006;355:2376–8.

    Article  PubMed  CAS  Google Scholar 

  93. Callera F, de Melo CM. Magnetic resonance tracking of magnetically labeled autologous bone marrow CD34+ cells transplanted into the spinal cord via lumbar puncture technique in patients with chronic spinal cord injury: CD34+ cells’ migration into the injured site. Stem Cells Dev. 2007;16:461–6.

    Article  PubMed  Google Scholar 

  94. Stroh A, Zimmer C, Werner N, Gertz K, Weir K, Kronenberg G, et al. Tracking of systemically administered mononuclear cells in the ischemic brain by high-field magnetic resonance imaging. Neuroimage. 2006;33:886–97.

    Article  PubMed  Google Scholar 

  95. Janowski M, Walczak P, Kropiwnicki T, Jurkiewicz E, Domanska-Janik K, Bulte JW, et al. Long-term MRI cell tracking after intraventricular delivery in a patient with global cerebral ischemia and prospects for magnetic navigation of stem cells within the CSF. PLoS One. 2014;9:e97631.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Hussain MA, Theise ND. Stem-cell therapy for diabetes mellitus. Lancet. 2004;364:203–5.

    Article  PubMed  Google Scholar 

  97. Voltarelli JC, Couri CE, Stracieri AB, Oliveira MC, Moraes DA, Pieroni F, et al. Autologous nonmyeloablative hematopoietic stem cell transplantation in newly diagnosed type 1 diabetes mellitus. JAMA. 2007;297:1568–76.

    Article  PubMed  CAS  Google Scholar 

  98. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation. Nature. 2004;429:41–6.

    Article  PubMed  CAS  Google Scholar 

  99. Tang K, Xiao X, Liu D, Shen Y, Chen Y, Wang Y, et al. Autografting of bone marrow mesenchymal stem cells alleviates streptozotocin-induced diabetes in miniature pigs: Real-time tracing with MRI in vivo. Int J Mol Med. 2014;33:1469–76.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Zhang B, Jiang B, Chen Y, Huang H, Xie Q, Kang M, et al. Detection of viability of transplanted beta cells labeled with a novel contrast agent–polyvinylpyrrolidone-coated superparamagnetic iron oxide nanoparticles by magnetic resonance imaging. Contrast Media Mol Imaging. 2012;7:35–44.

    Article  PubMed  Google Scholar 

  101. Orth P, Rey-Rico A, Venkatesan JK, Madry H, Cucchiarini M. Current perspectives in stem cell research for knee cartilage repair. Stem Cells Cloning. 2014;7:1–17.

    PubMed  PubMed Central  Google Scholar 

  102. Jing XH, Yang L, Duan XJ, Xie B, Chen W, Li Z, et al. 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. 2008;75:432–8.

    Article  PubMed  Google Scholar 

  103. Cromer Berman SM, Walczak P, Bulte JW. Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2011;3:343–55.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Medicine, Jiroft University of Medical Sciences, Jiroft, 8813833435, Iran

    Rasoul Yahyapour

  2. Department of Medical Physics and Radiology, Faculty of Paramedical Sciences, Kashan University of Medical Sciences, Kashan, 3715835155, Iran

    Bagher Farhood

  3. Department of Medical Physics and Biomedical Engineering, Faculty of Medicine, Tehran University of Medical Sciences, Tehran, 1417613151, Iran

    Ghazale Graily

  4. Department of Medical Physics, School of Medicine, Iran University of Medical Sciences, Tehran, 1449614535, Iran

    Abolhasan Rezaeyan & Hamid Abdollahi

  5. Department of Radiology, Faculty of Paramedical, Tehran University of Medical Sciences, Tehran, 1417613151, Iran

    Saeed Rezapoor & Peyman Amini

  6. Department of Radiologic Technology, Faculty of Paramedicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, 6135715794, Iran

    Mohsen Cheki

  7. Department of Chemistry, Faculty of Science, Islamic Azad University, Arak, 3836119131, Iran

    Hengameh Fallah

  8. Radiology and Nuclear Medicine Department, School of Paramedical Sciences, Kermanshah University of Medical Science, Kermanshah, 6714869914, Iran

    Masoud Najafi

  9. Department of Molecular Medicine, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, 194193311, Iran

    Elahe Motevaseli

Authors
  1. Rasoul Yahyapour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bagher Farhood
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ghazale Graily
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abolhasan Rezaeyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Saeed Rezapoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hamid Abdollahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mohsen Cheki
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Peyman Amini
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hengameh Fallah
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Masoud Najafi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Elahe Motevaseli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Masoud Najafi or Elahe Motevaseli.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

There are no animal or human experiments carried out for this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yahyapour, R., Farhood, B., Graily, G. et al. Stem Cell Tracing Through MR Molecular Imaging. Tissue Eng Regen Med 15, 249–261 (2018). https://doi.org/10.1007/s13770-017-0112-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13770-017-0112-8

Keywords

Search

Navigation