About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 849819, 16 pages
http://dx.doi.org/10.1155/2013/849819
Review Article

Multimodality Molecular Imaging of Stem Cells Therapy for Stroke

Fangfang Chao,1,2,3,4 Yehua Shen,1,2,3,4 Hong Zhang,1,2,3,4 and Mei Tian1,2,3,4

1Department of Nuclear Medicine, Second Affiliated Hospital of Zhejiang University School of Medicine, 88 Jiefang Road, Hangzhou, 310009 Zhejiang, China
2Zhejiang University Medical PET Center, Zhejiang University, Hangzhou, China
3Institute of Nuclear Medicine and Molecular Imaging, Zhejiang University, Hangzhou, China
4Key Laboratory of Medical Molecular Imaging of Zhejiang Province, Hangzhou, China

Received 20 April 2013; Accepted 21 August 2013

Academic Editor: Ignasi Carrio

Copyright © 2013 Fangfang Chao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. A. Donnan, M. Fisher, M. Macleod, and S. M. Davis, “Stroke,” The Lancet, vol. 371, no. 9624, pp. 1612–1623, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Wahlgren, N. Ahmed, A. Dávalos et al., “Thrombolysis with alteplase 3-4·5 h after acute ischaemic stroke (SITS-ISTR): an observational study,” The Lancet, vol. 372, no. 9646, pp. 1303–1309, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Berlis, H. Lutsep, S. Barnwell et al., “Mechanical thrombolysis in acute ischemic stroke with endovascular photoacoustic recanalization,” Stroke, vol. 35, no. 5, pp. 1112–1116, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Jin, Y. Sun, L. Xie et al., “Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intraventricular, or intravenous transplantation in the rat,” Neurobiology of Disease, vol. 18, no. 2, pp. 366–374, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. S. I. Savitz, M. Chopp, R. Deans, S. T. Carmichael, D. Phinney, and L. Wechsler, “Stem cell therapy as an emerging paradigm for stroke (STEPS) II,” Stroke, vol. 42, no. 3, pp. 825–829, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. J.-P. Lee, M. Jeyakumar, R. Gonzalez et al., “Stem cells act through multiple mechanisms to benefit mice with neurodegenerative metabolic disease,” Nature Medicine, vol. 13, no. 4, pp. 439–447, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. M. M. Daadi and G. K. Steinberg, “Manufacturing neurons from human embryonic stem cells: biological and regulatory aspects to develop a safe cellular product for stroke cell therapy,” Regenerative Medicine, vol. 4, no. 2, pp. 251–263, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Bliss, R. Guzman, M. Daadi, and G. K. Steinberg, “Cell transplantation therapy for stroke,” Stroke, vol. 38, supplement 2, pp. 817–826, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. M. Daadi, Z. Li, A. Arac et al., “Molecular and magnetic resonance imaging of human embryonic stem cell-derived neural stem cell grafts in ischemic rat brain,” Molecular Therapy, vol. 17, no. 7, pp. 1282–1291, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. E. M. Shapiro, K. Sharer, S. Skrtic, and A. P. Koretsky, “In vivo detection of single cells by MRI,” Magnetic Resonance in Medicine, vol. 55, no. 2, pp. 242–249, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. V. Mani, E. Adler, K. C. Briley-Saebo et al., “Serial in vivo positive contrast MRI of iron oxide-labeled embryonic stem cell-derived cardiac precursor cells in a mouse model of myocardial infarction,” Magnetic Resonance in Medicine, vol. 60, no. 1, pp. 73–81, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Amsalem, Y. Mardor, M. S. Feinberg et al., “Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium,” Circulation, vol. 116, supplement 11, pp. I38–I45, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. M. M. Daadi, S. Hu, J. Klausner, et al., “Imaging neural stem cell graft-induced structural repair in stroke,” Cell Transplantation, vol. 22, no. 5, pp. 881–892, 2013. View at Publisher · View at Google Scholar
  14. D. J. Chang, N. Lee, I. H. Park, et al., “Therapeutic potential of human induced pluripotent stem cells in experimental stroke,” Cell Transplantation, vol. 22, no. 8, pp. 1427–1440, 2013. View at Publisher · View at Google Scholar
  15. M. Srinivas, A. Heerschap, E. T. Ahrens, C. G. Figdor, and I. J. M. de Vries, “19F MRI for quantitative in vivo cell tracking,” Trends in Biotechnology, vol. 28, no. 7, pp. 363–370, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Modo, J. S. Beech, T. J. Meade, S. C. R. Williams, and J. Price, “A chronic 1 year assessment of MRI contrast agent-labelled neural stem cell transplants in stroke,” NeuroImage, vol. 47, supplement 2, pp. T133–T142, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. S. J. Zhang and J. C. Wu, “Comparison of imaging techniques for tracking cardiac stem cell therapy,” Journal of Nuclear Medicine, vol. 48, no. 12, pp. 1916–1919, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Darkazalli and C. W. Levenson, “Tracking stem cell migration and survival in brain injury: current approaches and future prospects,” Histol Histopathol, vol. 27, no. 10, pp. 1255–1261, 2012.
  19. T. Helmberger and R. C. Semelka, “New contrast agents for imaging the liver,” Magnetic Resonance Imaging Clinics of North America, vol. 9, no. 4, pp. 745–766, 2001. View at Scopus
  20. D. A. Hammoud, J. M. Hoffman, and M. G. Pomper, “Molecular neuroimaging: from conventional to emerging techniques,” Radiology, vol. 245, no. 1, pp. 21–42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Modo, “Understanding stem cell-mediated brain repair through neuroimaging,” Current Stem Cell Research & Therapy, vol. 1, no. 1, pp. 55–63, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Weber, S. Wegener, P. Ramos-Cabrer, D. Wiedermann, and M. Hoehn, “MRI detection of macrophage activity after experimental stroke in rats: new indicators for late appearance of vascular degradation?” Magnetic Resonance in Medicine, vol. 54, no. 1, pp. 59–66, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Guzman, N. Uchida, T. M. Bliss et al., “Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 24, pp. 10211–10216, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Neri, C. Maderna, C. Cavazzin et al., “Efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: relevance for in vivo cell tracking,” Stem Cells, vol. 26, no. 2, pp. 505–516, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. U. Himmelreich and T. Dresselaers, “Cell labeling and tracking for experimental models using Magnetic Resonance Imaging,” Methods, vol. 48, no. 2, pp. 112–124, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Hoehn, E. Küstermann, J. Blunk et al., “Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 25, pp. 16267–16272, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Zhu, L. Zhou, and F. XingWu, “Tracking neural stem cells in patients with brain trauma,” The New England Journal of Medicine, vol. 355, no. 22, pp. 2376–2378, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Doetsch, J. M. García-Verdugo, and A. Alvarez-Buylla, “Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain,” Journal of Neuroscience, vol. 17, no. 13, pp. 5046–5061, 1997. View at Scopus
  29. P.-M. Lledo, F. T. Merkle, and A. Alvarez-Buylla, “Origin and function of olfactory bulb interneuron diversity,” Trends in Neurosciences, vol. 31, no. 8, pp. 392–400, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Granot, D. Scheinost, E. A. Markakis, X. Papademetris, and E. M. Shapiro, “Serial monitoring of endogenous neuroblast migration by cellular MRI,” NeuroImage, vol. 57, no. 3, pp. 817–824, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. B. J. Nieman, J. Y. Shyu, J. J. Rodriguez, A. Denise Garcia, A. L. Joyner, and D. H. Turnbull, “In vivo MRI of neural cell migration dynamics in the mouse brain,” NeuroImage, vol. 50, no. 2, pp. 456–464, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Boehm-Sturm, L. Mengler, S. Wecker, M. Hoehn, and T. Kallur, “In vivo tracking of human neural stem cells with 19F magnetic resonance imaging,” PLoS One, vol. 6, no. 12, Article ID e29040, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. B. M. Helfer, A. Balducci, A. D. Nelson et al., “Functional assessment of human dendritic cells labeled for in vivo 19F magnetic resonance imaging cell tracking,” Cytotherapy, vol. 12, no. 2, pp. 238–250, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. E. T. Ahrens, R. Flores, H. Xu, and P. A. Morel, “In vivo imaging platform for tracking immunotherapeutic cells,” Nature Biotechnology, vol. 23, no. 8, pp. 983–987, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Genove, U. DeMarco, H. Xu, W. F. Goins, and E. T. Ahrens, “A new transgene reporter for in vivo magnetic resonance imaging,” Nature Medicine, vol. 11, no. 4, pp. 450–454, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Gera, G. K. Steinberg, and R. Guzman, “In vivo neural stem cell imaging: current modalities and future directions,” Regenerative Medicine, vol. 5, no. 1, pp. 73–86, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. O. Zurkiya, A. W. S. Chan, and X. Hu, “MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter,” Magnetic Resonance in Medicine, vol. 59, no. 6, pp. 1225–1231, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. P. D. Acton and R. Zhou, “Imaging reporter genes for cell tracking with PET and SPECT,” Quarterly Journal of Nuclear Medicine and Molecular Imaging, vol. 49, no. 4, pp. 349–360, 2005. View at Scopus
  39. K. J. Blackwood, B. Lewden, R. G. Wells et al., “In vivo SPECT quantification of transplanted cell survival after engraftment using 111In-tropolone in infarcted canine myocardium,” Journal of Nuclear Medicine, vol. 50, no. 6, pp. 927–935, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Huang, C. C. I. Lee, J. L. Sutcliffe, S. R. Cherry, and A. F. Tarantal, “Radiolabeling Rhesus monkey CD34+ hematopoietic and mesenchymal stem cells with 64Cu-pyruvaldehyde-bis(N4-methylthiosemicarbazone) for MicroPET imaging,” Molecular Imaging, vol. 7, no. 1, pp. 1–11, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. G. V. Goldmacher, R. Nasser, D. Y. Lee, S. Yigit, R. Rosenwasser, and L. Iacovitti, “Tracking transplanted bone marrow stem cells and their effects in the rat MCAO stroke model,” PLoS One, vol. 8, no. 3, Article ID e60049, 2013.
  42. J. A. Gleave, J. F. Valliant, and L. C. Doering, “99mTc-Based imaging of transplanted neural stem cells and progenitor cells,” Journal of Nuclear Medicine Technology, vol. 39, no. 2, pp. 114–120, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Gu, W. Y. Chen, J. Gu, P. Burridge, and J. C. Wu, “Molecular imaging of stem cells: tracking survival, biodistribution, tumorigenicity, and immunogenicity,” Theranostics, vol. 2, no. 4, pp. 335–345, 2012. View at Publisher · View at Google Scholar
  44. E. R. Chemaly, R. Yoneyama, J. V. Frangioni, and R. J. Hajjar, “Tracking stem cells in the cardiovascular system,” Trends in Cardiovascular Medicine, vol. 15, no. 8, pp. 297–302, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Jiang, Z. Cheng, M. Tian, and H. Zhang, “In vivo imaging of embryonic stem cell therapy,” European Journal of Nuclear Medicine and Molecular Imaging, vol. 38, no. 4, pp. 774–784, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Yaghoubi, J. R. Barrio, M. Dahlbom et al., “Human pharmacokinetic and dosimetry studies of [18F]FHBG: a reporter probe for imaging herpes simplex virus type-1 thymidine kinase reporter gene expression,” Journal of Nuclear Medicine, vol. 42, no. 8, pp. 1225–1234, 2001. View at Scopus
  47. Y. Persidsky, S. H. Ramirez, J. Haorah, and G. D. Kanmogne, “Blood-brain barrier: structural components and function under physiologic and pathologic conditions,” Journal of Neuroimmune Pharmacology, vol. 1, no. 3, pp. 223–236, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. R. A. Kroll and E. A. Neuwelt, “Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means,” Neurosurgery, vol. 42, no. 5, pp. 1083–1100, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Iyer, J. R. Barrio, M. Namavari et al., “8-[18F]fluoropenciclovir: an improved reporter probe for imaging HSV1-tk reporter gene expression in vivo using PET,” Journal of Nuclear Medicine, vol. 42, no. 1, pp. 96–105, 2001. View at Scopus
  50. F. Cao, S. Lin, X. Xie et al., “In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery,” Circulation, vol. 113, no. 7, pp. 1005–1014, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. G. Y. Chang, F. Cao, M. Krishnan et al., “Positron emission tomography imaging of conditional gene activation in the heart,” Journal of Molecular and Cellular Cardiology, vol. 43, no. 1, pp. 18–26, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Waerzeggers, M. Klein, H. Miletic et al., “Multimodal imaging of neural progenitor cell fate in rodents,” Molecular Imaging, vol. 7, no. 2, pp. 77–91, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. S. S. Yaghoubi, M. C. Jensen, N. Satyamurthy et al., “Noninvasive detection of therapeutic cytolytic T cells with 18 F-FHBG PET in a patient with glioma,” Nature Clinical Practice Oncology, vol. 6, no. 1, pp. 53–58, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Wu, J. Lang, X. Sun, B. Zhang, Y. Liu, and R. An, “Monitoring bone marrow stem cells with a reporter gene system in experimental middle cerebral artery occlusion rat models,” Journal of Nuclear Medicine, vol. 54, no. 6, pp. 984–989, 2013.
  55. D. R. LeMay, M. Kittaka, E. M. Gordon et al., “Intravenous RMP-7 increases delivery of ganciclovir into rat brain tumors and enhances the effects of herpes simplex virus thymidine kinase gene therapy,” Human Gene Therapy, vol. 9, no. 7, pp. 989–995, 1998. View at Scopus
  56. M. Doubrovin, V. Ponomarev, I. Serganova et al., “Development of a new reporter gene system-dsRed/Xanthine phosphoribosyltransferase-xanthine for molecular imaging of processes behind the intact blood-brain barrier,” Molecular Imaging, vol. 2, no. 2, pp. 93–112, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. J. R. Barrio, N. Satyamurthy, S.-C. Huang et al., “3-(2′-[18F]fluoroethyl)spiperone: in vivo biochemical and kinetic characterization in rodents, nonhuman primates, and humans,” Journal of Cerebral Blood Flow and Metabolism, vol. 9, no. 6, pp. 830–839, 1989. View at Scopus
  58. D. C. MacLaren, S. S. Gambhir, N. Satyamurthy et al., “Repetitive, non-invasive imaging of the dopamine D2 receptor as a reporter gene in living animals,” Gene Therapy, vol. 6, no. 5, pp. 785–791, 1999. View at Publisher · View at Google Scholar · View at Scopus
  59. S. S. Yaghoubi, L. Wu, Q. Liang et al., “Direct correlation between positron emission tomographic images of two reporter genes delivered by two distinct adenoviral vectors,” Gene Therapy, vol. 8, no. 14, pp. 1072–1080, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. J. H. Shin, J.-K. Chung, J. H. Kang et al., “Feasibility of sodium/iodide symporter gene as a new imaging reporter gene: comparison with HSV1-tk,” European Journal of Nuclear Medicine and Molecular Imaging, vol. 31, no. 3, pp. 425–432, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. C. Qin, K. Cheng, K. Chen, et al., “Tyrosinase as a multifunctional reporter gene for Photoacoustic/MRI/PET triple modality molecular imaging,” Scientific Reports, vol. 3, p. 1490, 2013.
  62. Y. Zhang, M. Ruel, R. S. B. Beanlands, R. A. deKemp, E. J. Suuronen, and J. N. DaSilva, “Tracking stem cell therapy in the myocardium: applications of positron emission tomography,” Current Pharmaceutical Design, vol. 14, no. 36, pp. 3835–3853, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. X.-B. Kong, Q.-Y. Zhu, P. M. Vidal et al., “Comparisons of anti-human immunodeficiency virus activities, cellular transport, and plasma and intracellular pharmacokinetics of 3′-fluoro-3′- deoxythymidine and 3′-azido-3′-deoxythymidine,” Antimicrobial Agents and Chemotherapy, vol. 36, no. 4, pp. 808–818, 1992. View at Scopus
  64. M. A. Rueger, H. Backes, M. Walberer et al., “Noninvasive imaging of endogenous neural stem cell mobilization in vivo using positron emission tomography,” Journal of Neuroscience, vol. 30, no. 18, pp. 6454–6460, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Couillard-Despres, R. Vreys, L. Aigner, and A. van der Linden, “In vivo monitoring of adult neurogenesis in health and disease,” Frontiers in Neuroscience, vol. 5, p. 67, 2011.
  66. J. Wang, F. Chao, F. Han, et al., “PET demonstrates functional recovery after transplantation of induced pluripotent stem cells in a rat model of cerebral ischemic injury,” Journal of Nuclear Medicine, vol. 54, no. 5, pp. 785–792, 2013. View at Publisher · View at Google Scholar
  67. M. Miyamoto, S. Kuroda, S. Zhao, et al., “Bone marrow stromal cell transplantation enhances recovery of local glucose metabolism after cerebral infarction in rats: a serial 18F-FDG PET study,” Journal of Nuclear Medicine, vol. 54, no. 1, pp. 145–150, 2013. View at Publisher · View at Google Scholar
  68. D. Kondziolka, L. Wechsler, S. Goldstein et al., “Transplantation of cultured human neuronal cells for patients with stroke,” Neurology, vol. 55, no. 4, pp. 565–569, 2000. View at Scopus
  69. S. Boddington, T. D. Henning, E. J. Sutton, and H. E. Daldrup-Link, “Labeling stem cells with fluorescent dyes for non-invasive detection with optical imaging,” Journal of Visualized Experiments, no. 14, article e686, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. C.-H. Tung, “Fluorescent peptide probes for in vivo diagnostic imaging,” Biopolymers, vol. 76, no. 5, pp. 391–403, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. P. Bossolasco, L. Cova, G. Levandis et al., “Noninvasive near-infrared live imaging of human adult mesenchymal stem cells transplanted in a rodent model of Parkinson's disease,” International Journal of Nanomedicine, vol. 7, pp. 435–447, 2012. View at Scopus
  72. X. Chen, P. S. Conti, and R. A. Moats, “In vivo near-infrared fluorescence imaging of integrin α vβ3 in brain tumor xenografts,” Cancer Research, vol. 64, no. 21, pp. 8009–8014, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Zhang, X. Tan, L. Tan et al., “Labeling stem cells with a near-infrared fluorescent heptamethine dye for noninvasive optical tracking,” Cell Transplantation, vol. 20, no. 5, pp. 741–751, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Sugiyama, S. Kuroda, T. Osanai et al., “Near-infrared fluorescence labeling allows noninvasive tracking of bone marrow stromal cells transplanted into rat infarct brain,” Neurosurgery, vol. 68, no. 4, pp. 1036–1047, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. J. K. Jaiswal, H. Mattoussi, J. M. Mauro, and S. M. Simon, “Long-term multiple color imaging of live cells using quantum dot bioconjugates,” Nature Biotechnology, vol. 21, no. 1, pp. 47–51, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. J. R. Slotkin, L. Chakrabarti, N. D. Hai et al., “In vivo quantum dot labeling of mammalian stem and progenitor cells,” Developmental Dynamics, vol. 236, no. 12, pp. 3393–3401, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Kawabori, S. Kuroda, T. Sugiyama et al., “Intracerebral, but not intravenous, transplantation of bone marrow stromal cells enhances functional recovery in rat cerebral infarct: an optical imaging study,” Neuropathology, vol. 32, no. 3, pp. 217–226, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. T. F. Massoud, A. Singh, and S. S. Gambhir, “Noninvasive molecular neuroimaging using reporter genes: part I, principles revisited,” American Journal of Neuroradiology, vol. 29, no. 2, pp. 229–234, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. K. Kruttwig, C. Brueggemann, E. Kaijzel et al., “Development of a three-dimensional in vitro model for longitudinal observation of cell behavior: monitoring by magnetic resonance imaging and optical imaging,” Molecular Imaging and Biology, vol. 12, no. 4, pp. 367–376, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. E. J. Sutton, T. D. Henning, B. J. Pichler, C. Bremer, and H. E. Daldrup-Link, “Cell tracking with optical imaging,” European Radiology, vol. 18, no. 10, pp. 2021–2032, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. D.-E. Kim, D. Schellingerhout, K. Ishii, K. Shah, and R. Weissleder, “Imaging of stem cell recruitment to ischemic infarcts in a murine model,” Stroke, vol. 35, no. 4, pp. 952–957, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. R. H. Andres, R. Choi, A. V. Pendharkar et al., “The CCR2/CCL2 interaction mediates the transendothelial recruitment of intravascularly delivered neural stem cells to the ischemic brain,” Stroke, vol. 42, no. 10, pp. 2923–2931, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. N. J. Robertson, F. A. Brook, R. L. Gardner, S. P. Cobbold, H. Waldmann, and P. J. Fairchild, “Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 52, pp. 20920–20925, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. R.-J. Swijnenburg, S. Schrepfer, J. A. Govaert et al., “Immunosuppressive therapy mitigates immunological rejection of human embryonic stem cell xenografts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 35, pp. 12991–12996, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. W. Su, M. Zhou, Y. Zheng et al., “Bioluminescence reporter gene imaging characterize human embryonic stem cell-derived teratoma formation,” Journal of Cellular Biochemistry, vol. 112, no. 3, pp. 840–848, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. V. Reumers, C. M. Deroose, O. Krylyshkina et al., “Noninvasive and quantitative monitoring of adult neuronal stem cell migration in mouse brain using bioluminescence imaging,” Stem Cells, vol. 26, no. 9, pp. 2382–2390, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Couillard-Despres, R. Finkl, B. Winner et al., “In vivo optical imaging of neurogenesis: watching new neurons in the intact brain,” Molecular Imaging, vol. 7, no. 1, pp. 28–34, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. A. Arvidsson, T. Collin, D. Kirik, Z. Kokaia, and O. Lindvall, “Neuronal replacement from endogenous precursors in the adult brain after stroke,” Nature Medicine, vol. 8, no. 9, pp. 963–970, 2002. View at Publisher · View at Google Scholar · View at Scopus
  89. P. Thored, A. Arvidsson, E. Cacci et al., “Persistent production of neurons from adult brain stem cells during recovery after stroke,” Stem Cells, vol. 24, no. 3, pp. 739–747, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. J. H. Kang and J. K. Chung, “Molecular-genetic imaging based on reporter gene expression,” Journal of Nuclear Medicine, vol. 49, supplement 2, pp. 164S–179S, 2008.
  91. W. J. M. Mulder, A. W. Griffioen, G. J. Strijkers, D. P. Cormode, K. Nicolay, and Z. A. Fayad, “Magnetic and fluorescent nanoparticles for multimodality imaging,” Nanomedicine, vol. 2, no. 3, pp. 307–324, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. R. Koole, W. J. M. Mulder, M. M. van Schooneveld, G. J. Strijkers, A. Meijerink, and K. Nicolay, “Magnetic quantum dots for multimodal imaging,” Wiley Interdisciplinary Reviews, vol. 1, no. 5, pp. 475–491, 2009. View at Publisher · View at Google Scholar · View at Scopus