Advances in using MRI probes and sensors for in vivo cell tracking as applied to regenerative medicine

DMM Disease Models and Mechanisms

Volumn 8, Issue 4, 2015, Pages 323-336

  Srivastava, Amit K ^a   Kadayakkara, Deepak K ^a   Bar Shir, Amnon ^a   Gilad, Assaf A ^a,b   McMahon, Michael T ^a,b   Bulte, Jeff W M ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

Biosensor; Cell labeling; Cellular function; CEST; Magnetic resonance imaging; Paramagnetic contrast agents; Perfluorocarbon particles; Regenerative medicine; Stem cells

Indexed keywords

CONTRAST MEDIUM; FLUORINE; FLUOROCARBON; GADOLINIUM; MANGANESE; MANGANESE OXIDE; METAL ION; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

BIOSENSOR; CELL DEATH; CELL FATE; CELL FUNCTION; CELL LABELING; CELL THERAPY; CELL TRACKING; CELL VIABILITY; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; IN VIVO STUDY; MECHANICAL PROBE; MOLECULAR IMAGING; NANOSENSOR; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PH; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REGENERATIVE MEDICINE; REVIEW; STEM CELL TRANSPLANTATION; ANIMAL; PROCEDURES; TRANSLATIONAL RESEARCH;

ANIMALS; CELL TRACKING; CONTRAST MEDIA; HUMANS; MAGNETIC RESONANCE IMAGING; REGENERATIVE MEDICINE; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84927509467     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.018499     Document Type: Review

References (179)

1. Agudelo, C. A., Tachibana, Y., Hurtado, A. F., Ose, T., Iida, H. and Yamaoka, T. (2012). The use of magnetic resonance cell tracking to monitor endothelial progenitor cells in a rat hindlimb ischemic model. Biomaterials 33, 2439-2448.
2. Ahrens, E. T. and Bulte, J. W. (2013). Tracking immune cells in vivo using magnetic resonance imaging. Nat. Rev. Immunol. 13, 755-763.
3. Ahrens, E. T. and Zhong, J. (2013). In vivo MRI cell tracking using perfluorocarbon probes and fluorine-19 detection. NMR Biomed. 26, 860-871.
4. Ahrens, E. T., and Helfer, B. M., O'Hanlon, C. F. and Schirda, C. (2014). Clinical cell therapy imaging using a perfluorocarbon tracer and fluorine-19 MRI. Magn. Reson. Med. 72, 1696-1701.
5. Aime, S., Delli Castelli, D. and Terreno, E. (2002). Novel pH-reporter MRI contrast agents. Angew. Chem. Int. Ed. Engl. 41, 4334-4336.
6. Aime, S., Carrera, C., Delli Castelli, D., Geninatti Crich, S. and Terreno, E. (2005). Tunable imaging of cells labeled with MRI-PARACEST agents. Angew. Chem. Int. Ed. Engl. 44, 1813-1815.
7. Airan, R. D., Bar-Shir, A., Liu, G., Pelled, G., McMahon, M. T., van Zijl, P. C., Bulte, J. W. and Gilad, A. A. (2012). MRI biosensor for protein kinase A encoded by a single synthetic gene. Magn. Reson. Med. 68, 1919-1923.
8. Airan, R. D., Li, N., Gilad, A. A. and Pelled, G. (2013). Genetic tools to manipulate MRI contrast. NMR Biomed. 26, 803-809.
9. Alfke, H., Stöppler, H., Nocken, F., and Heverhagen, J. T., Kleb, B., Czubayko, F. and Klose, K. J. (2003). In vitro MR imaging of regulated gene expression. Radiology 228, 488-492.
10. Aoki, I., Takahashi, Y., Chuang, K. H., and Silva, A. C., Igarashi, T., Tanaka, C., Childs, R. W. and Koretsky, A. P. (2006). Cell labeling for magnetic resonance imaging with the T1 agent manganese chloride. NMR Biomed. 19, 50-59.
11. Atanasijevic, T., Shusteff, M., Fam, P. and Jasanoff, A. (2006). Calcium-sensitive MRI contrast agents based on superparamagnetic iron oxide nanoparticles and calmodulin. Proc. Natl. Acad. Sci. USA 103, 14707-14712.
12. Bandmann, O., Weiss, K. H. and Kaler, S. G. (2015). Wilson's disease and other neurological copper disorders. Lancet Neurol. 14, 103-113.
13. Bar-Shir, A., Gilad, A. A., and Chan, K. W., Liu, G., van Zijl, P. C., Bulte, J. W. and McMahon, M. T. (2013a). Metal ion sensing using ion chemical exchange saturation transfer 19F magnetic resonance imaging. J. Am. Chem. Soc. 135, 12164-12167.
14. Bar-Shir, A., Liu, G., and Greenberg, M. M., Bulte, J. W. M. and Gilad, A. A. (2013b). Synthesis of a probe for monitoring HSV1-tk reporter gene expression using chemical exchange saturation transfer MRI. Nat. Protoc. 8, 2380-2391.
15. Bar-Shir, A., Liu, G., Liang, Y., Yadav, N. N., and McMahon, M. T., Walczak, P., Nimmagadda, S., Pomper, M. G., Tallman, K. A., Greenberg, M. M. et al. (2013c). Transforming thymidine into a magnetic resonance imaging probe for monitoring gene expression. J. Am. Chem. Soc. 135, 1617-1624.
16. Bar-Shir, A., Liu, G., and Chan, K. W., Oskolkov, N., Song, X., Yadav, N. N., Walczak, P., and McMahon, M. T., van Zijl, P. C., Bulte, J. W. et al. (2014). Human protamine-1 as an MRI reporter gene based on chemical exchange. ACS Chem. Biol. 9, 134-138.
17. Bar-Shir, A., Yadav, N. N., and Gilad, A. A., van Zijl, P. C., McMahon, M. T. and Bulte, J. W. (2015). Single (19)F Probe for Simultaneous Detection of Multiple Metal Ions Using miCEST MRI. J. Am. Chem. Soc. 137, 78-81.
18. Barnett, B. P., Arepally, A., Karmarkar, P. V., Qian, D., and Gilson, W. D., Walczak, P., Howland, V., Lawler, L., Lauzon, C., Stuber, M. et al. (2007). Magnetic resonance-guided, real-time targeted delivery and imaging of magnetocapsules immunoprotecting pancreatic islet cells. Nat. Med. 13, 986-991.
19. Barnett, B. P., Ruiz-Cabello, J., Hota, P., Ouwerkerk, R., Shamblott, M. J., Lauzon, C., Walczak, P., Gilson, W. D., Chacko, V. P., Kraitchman, D. L. et al. (2011). Use of perfluorocarbon nanoparticles for non-invasive multimodal cell tracking of human pancreatic islets. Contrast Media Mol. Imaging 6, 251-259.
20. Barsotti, M. C., Felice, F., Balbarini, A. and Di Stefano, R. (2011). Fibrin as a scaffold for cardiac tissue engineering. Biotechnol. Appl. Biochem. 58, 301-310.
21. Bartelle, B. B., Berríos-Otero, C. A., Rodriguez, J. J., Friedland, A. E., Aristizábal, O. and Turnbull, D. H. (2012). Novel genetic approach for in vivo vascular imaging in mice. Circ. Res. 110, 938-947.
22. Bartelle, B. B., and Szulc, K. U., Suero-Abreu, G. A., Rodriguez, J. J. and Turnbull, D. H. (2013). Divalent metal transporter, DMT1: A novel MRI reporter protein. Magn. Reson. Med. 70, 842-850.
23. Bastiaansen, J. A., Cheng, T., Mishkovsky, M., Duarte, J. M., Comment, A. and Gruetter, R. (2013). In vivo enzymatic activity of acetylCoA synthetase in skeletal muscle revealed by (13)C turnover from hyperpolarized [1-(13)C]acetate to [1-(13)C]acetylcarnitine. Biochim. Biophys. Acta 1830, 4171-4178.
24. Bhorade, R., Weissleder, R., Nakakoshi, T., Moore, A. and Tung, C. H. (2000). Macrocyclic chelators with paramagnetic cations are internalized into mammalian cells via a HIV-tat derived membrane translocation peptide. Bioconjug. Chem. 11, 301-305.
25. Bible, E., Dell'Acqua, F., Solanky, B., Balducci, A., Crapo, P. M., Badylak, S. F., Ahrens, E. T. and Modo, M. (2012). Non-invasive imaging of transplanted human neural stem cells and ECM scaffold remodeling in the stroke-damaged rat brain by (19)F- and diffusion-MRI. Biomaterials 33, 2858-2871.
26. Bloch, F., Hansen, W. W. and Packard, M. (1946). Nuclear induction. Phys. Rev. 69, 127.
27. Boehm-Sturm, P., Mengler, L., Wecker, S., Hoehn, M. and Kallur, T. (2011). In vivo tracking of human neural stem cells with 19F magnetic resonance imaging. PLoS ONE 6, e29040.
28. Bottomley, P. A., and Hart, H. R., Edelstein, W. A., Schenck, J. F., and Smith, L. S., Leue, W. M., Mueller, O. M. and Redington, R. W. (1983). NMR imaging/spectroscopy system to study both anatomy and metabolism. Lancet 322, 273-274.
29. Brennan, M. L., and Penn, M. S., Van Lente, F., Nambi, V., Shishehbor, M. H., and Aviles, R. J., Goormastic, M., Pepoy, M. L., McErlean, E. S., Topol, E. J. et al. (2003). Prognostic value of myeloperoxidase in patients with chest pain. N. Engl. J. Med. 349, 1595-1604.
30. Bulte, J. W. (2005). Hot spot MRI emerges from the background. Nat. Biotechnol. 23, 945-946.
31. Bulte, J. W. (2009). In vivo MRI cell tracking: clinical studies. AJR Am. J. Roentgenol. 193, 314-325.
32. Bulte, J. W. (2014). Science to practice: highly shifted proton MR imaging - a shift toward better cell tracking? Radiology 272, 615-617.
33. Bulte, J. W. and Kraitchman, D. L. (2004). Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 17, 484-499.
34. Bulte, J. W., Hoekstra, Y., Kamman, R. L., and Magin, R. L., Webb, A. G., Briggs, R. W., Go, K. G., Hulstaert, C. E., Miltenyi, S., The, T. H. et al. (1992). Specific MR imaging of human lymphocytes by monoclonal antibody-guided dextran-magnetite particles. Magn. Reson. Med. 25, 148-157.
35. Bulte, J. W., and Ma, L. D., Magin, R. L., Kamman, R. L., and Hulstaert, C. E., Go, K. G., The, T. H. and de Leij, L. (1993). Selective MR imaging of labeled human peripheral blood mononuclear cells by liposome mediated incorporation of dextran-magnetite particles. Magn. Reson. Med. 29, 32-37.
36. Bulte, J. W., Douglas, T., Witwer, B., Zhang, S. C., Strable, E., and Lewis, B. K., Zywicke, H., Miller, B., van Gelderen, P., Moskowitz, B. M. et al. (2001). Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat. Biotechnol. 19, 1141-1147.
37. Bulte, J. W., and Kraitchman, D. L., Mackay, A. M. and Pittenger, M. F. (2004). Chondrogenic differentiation of mesenchymal stem cells is inhibited after magnetic labeling with ferumoxides. Blood 104, 3410-3412, author reply 3412-3413.
38. Catanzaro, V., and Gringeri, C. V., Menchise, V., Padovan, S., Boffa, C., Dastrù, W., Chaabane, L., Digilio, G. and Aime, S. (2013). A R2p /R1p ratiometric procedure to assess matrix metalloproteinase-2 activity by magnetic resonance imaging. Angew. Chem. Int. Ed. Engl. 52, 3926-3930.
39. Chan, K. W., Liu, G., Song, X., Kim, H., Yu, T., Arifin, D. R., Gilad, A. A., Hanes, J., Walczak, P., van Zijl, P. C. et al. (2013). MRI-detectable pH nanosensors incorporated into hydrogels for in vivo sensing of transplanted-cell viability. Nat. Mater. 12, 268-275.
40. Chen, J. W., Pham, W., Weissleder, R. and Bogdanov, A., Jr (2004). Human myeloperoxidase: a potential target for molecular MR imaging in atherosclerosis. Magn. Reson. Med. 52, 1021-1028.
41. Chen, A. P., and Hurd, R. E., Gu, Y. P., Wilson, D. M. and Cunningham, C. H. (2011). (13)C MR reporter probe system using dynamic nuclear polarization. NMR Biomed. 24, 514-520.
42. Cohen, B., Dafni, H., Meir, G., Harmelin, A. and Neeman, M. (2005). Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6 glioma tumors. Neoplasia 7, 109-117.
43. Cohen, B., Ziv, K., Plaks, V., Israely, T., Kalchenko, V., Harmelin, A., Benjamin, L. E. and Neeman, M. (2007). MRI detection of transcriptional regulation of gene expression in transgenic mice. Nat. Med. 13, 498-503.
44. Cromer Berman, S. M., Walczak, P. and Bulte, J. W. (2011). Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 3, 343-355.
45. Cromer Berman, S. M., Kshitiz, Wang, C. J., Orukari, I., Levchenko, A., Bulte, J. W. and Walczak, P. (2013). Cell motility of neural stem cells is reduced after SPIO-labeling, which is mitigated after exocytosis. Magn. Reson. Med. 69, 255-262.
46. Cui, W., Otten, P., Li, Y., Koeneman, K. S., Yu, J. and Mason, R. P. (2004). Novel NMR approach to assessing gene transfection: 4-fluoro-2-nitrophenyl-beta-D-galactopyranoside as a prototype reporter molecule for beta-galactosidase. Magn. Reson. Med. 51, 616-620.
47. Damadian, R. (1971). Tumor detection by nuclear magnetic resonance. Science 171, 1151-1153.
48. de Vries, I. J., Lesterhuis, W. J., and Barentsz, J. O., Verdijk, P., van Krieken, J. H., Boerman, O. C., Oyen, W. J., Bonenkamp, J. J., Boezeman, J. B., Adema, G. J. et al. (2005). Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat. Biotechnol. 23, 1407-1413.
49. Deans, A. E., and Wadghiri, Y. Z., Bernas, L. M., Yu, X., Rutt, B. K. and Turnbull, D. H. (2006). Cellular MRI contrast via coexpression of transferrin receptor and ferritin. Magn. Reson. Med. 56, 51-59.
50. Dickinson, W. C. (1950). Dependence of the F19 nuclear resonance position on chemical compound. Phys. Rev. 77, 736.
51. Duimstra, J. A., Femia, F. J. and Meade, T. J. (2005). A gadolinium chelate for detection of beta-glucuronidase: a self-immolative approach. J. Am. Chem. Soc. 127, 12847-12855.
52. Esqueda, A. C., López, J. A., Andreu-de-Riquer, G., Alvarado-Monzón, J. C., Ratnakar, J., Lubag, A. J., Sherry, A. D. and De León-Rodríguez, L. M. (2009). A new gadolinium-based MRI zinc sensor. J. Am. Chem. Soc. 131, 11387-11391.
53. Ferrauto, G., Delli Castelli, D., Terreno, E. and Aime, S. (2013). In vivo MRI visualization of different cell populations labeled with PARACEST agents. Magn. Reson. Med. 69, 1703-1711.
54. Frank, J. A., Zywicke, H., Jordan, E. K., Mitchell, J., and Lewis, B. K., Miller, B., Bryant, L. H., Jr and Bulte, J. W. (2002). 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.
55. Genove, G., DeMarco, U., Xu, H., Goins, W. F. and Ahrens, E. T. (2005). A new transgene reporter for in vivo magnetic resonance imaging. Nat. Med. 11, 450-454.
56. Ghaghada, K. B., Ravoori, M., Sabapathy, D., Bankson, J., Kundra, V. and Annapragada, A. (2009). New dual mode gadolinium nanoparticle contrast agent for magnetic resonance imaging. PLoS ONE 4, e7628.
57. Gilad, A. A., and McMahon, M. T., Walczak, P., Winnard, P. T., Jr, Raman, V., van Laarhoven, H. W., Skoglund, C. M., Bulte, J. W. and van Zijl, P. C. (2007a). Artificial reporter gene providing MRI contrast based on proton exchange. Nat. Biotechnol. 25, 217-219.
58. Gilad, A. A., and Winnard, P. T., Jr, van Zijl, P. C. and Bulte, J. W. (2007b). Developing MR reporter genes: promises and pitfalls. NMR Biomed. 20, 275-290.
59. Gilad, A. A., Walczak, P., McMahon, M. T., and Na, H. B., Lee, J. H., An, K., Hyeon, T., van Zijl, P. C. and Bulte, J. W. (2008a). MR tracking of transplanted cells with "positive contrast" using manganese oxide nanoparticles. Magn. Reson. Med. 60, 1-7.
60. Gilad, A. A., Ziv, K., McMahon, M. T., van Zijl, P. C., Neeman, M. and Bulte, J. W. (2008b). MRI reporter genes. J. Nucl. Med. 49, 1905-1908.
61. Gillies, R. J., Liu, Z. and Bhujwalla, Z. (1994). 31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate. Am. J. Physiol. 267, C195-C203.
62. Gillies, R. J., Raghunand, N., Garcia-Martin, M. L. and Gatenby, R. A. (2004). pH imaging. A review of pH measurement methods and applications in cancers. IEEE Eng. Med. Biol. Mag. 23, 57-64.
63. Gomathysankar, S., Halim, A. S. and Yaacob, N. S. (2014). Proliferation of keratinocytes induced by adipose-derived stem cells on a chitosan scaffold and its role in wound healing, a review. Arch. Plast. Surg. 41, 452-457.
64. Gottesfeld, Z. and Neeman, M. (1996). Ferritin effect on the transverse relaxation of water: NMR microscopy at 9.4 T. Magn. Reson. Med. 35, 514-520.
65. Guenoun, J., and Koning, G. A., Doeswijk, G., Bosman, L., Wielopolski, P. A., Krestin, G. P. and Bernsen, M. R. (2012). Cationic Gd-DTPA liposomes for highly efficient labeling of mesenchymal stem cells and cell tracking with MRI. Cell Transplant. 21, 191-205.
66. Haris, M., Singh, A., Cai, K., Kogan, F., McGarvey, J., Debrosse, C., Zsido, G. A., Witschey, W. R., Koomalsingh, K., Pilla, J. J. et al. (2014). A technique for in vivo mapping of myocardial creatine kinase metabolism. Nat. Med. 20, 209-214.
67. Hawrylak, N., Ghosh, P., Broadus, J., Schlueter, C., Greenough, W. T. and Lauterbur, P. C. (1993). Nuclear magnetic resonance (NMR) imaging of iron oxide-labeled neural transplants. Exp. Neurol. 121, 181-192.
68. 3 nanoparticles in hematopoietic cells for MRI contrast enhancement. Int. J. Nanomedicine 6, 3233-3240.
69. Hifumi, H., Tanimoto, A., Citterio, D., Komatsu, H. and Suzuki, K. (2007). Novel 15-crown-5 ether or beta-diketone incorporated gadolinium complexes for the detection of potassium ions or magnesium and calcium ions. Analyst 132, 1153-1160.
70. Hingorani, D. V., Randtke, E. A. and Pagel, M. D. (2013). A cataly CEST MRI contrast agent that detects the enzyme-catalyzed creation of a covalent bond. J. Am. Chem. Soc. 135, 6396-6398.
71. Holland, G. N., Bottomley, P. A. and Hinshaw, W. S. (1977). 19F Magnetic Resonance Imaging. J. Magn. Reson. 28, 133-136.
72. Hounsfield, G. N. (1973). Computerized transverse axial scanning (tomography). 1. Description of system. Br. J. Radiol. 46, 1016-1022.
73. Iordanova, B. and Ahrens, E. T. (2012). In vivo magnetic resonance imaging of ferritin-based reporter visualizes native neuroblast migration. Neuroimage 59, 1004-1012.
74. Iordanova, B., Robison, C. S. and Ahrens, E. T. (2010). Design and characterization of a chimeric ferritin with enhanced iron loading and transverse NMR relaxation rate. J. Biol. Inorg. Chem. 15, 957-965.
75. Jamin, Y., Gabellieri, C., Smyth, L., Reynolds, S., and Robinson, S. P., Springer, C. J., Leach, M. O., Payne, G. S. and Eykyn, T. R. (2009). Hyperpolarized (13)C magnetic resonance detection of carboxypeptidase G2 activity. Magn. Reson. Med. 62, 1300-1304.
76. Jamin, Y., and Eykyn, T. R., Poon, E., Springer, C. J. and Robinson, S. P. (2013). Detection of the prodrug-activating enzyme carboxypeptidase G2 activity with chemical exchange saturation transfer magnetic resonance. Mol. Imaging Biol. 60, 1-7
77. Janjic, J. M. and Ahrens, E. T. (2009). Fluorine-containing nanoemulsions for MRI cell tracking. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 1, 492-501.
78. Janowski, M., Walczak, P., Kropiwnicki, T., Jurkiewicz, E., Domanska-Janik, K., Bulte, J. W., Lukomska, B. and Roszkowski, M. (2014). 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 9, e97631.
79. Kadayakkara, D. K., and Janjic, J. M., Pusateri, L. K., Young, W. B. and Ahrens, E. T. (2010). In vivo observation of intracellular oximetry in perfluorocarbon-labeled glioma cells and chemotherapeutic response in the CNS using fluorine-19 MRI. Magn. Reson. Med. 64, 1252-1259.
80. Kadayakkara, D. K., Damodaran, K., Hitchens, T. K., Bulte, J. W. and Ahrens, E. T. (2014). (19)F spin-lattice relaxation of perfluoropolyethers: Dependence on temperature and magnetic field strength (7.0-14.1T). J. Magn. Reson. 242, 18-22.
81. Karussis, D., Karageorgiou, C., Vaknin-Dembinsky, A., Gowda-Kurkalli, B., Gomori, J. M., Kassis, I., Bulte, J. W., Petrou, P., Ben-Hur, T., Abramsky, O. et al. (2010). Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch. Neurol. 67, 1187-1194.
82. Keupp, J., Rahmer, J., Grässlin, I., Mazurkewitz, P. C., Schaeffter, T., and Lanza, G. M., Wickline, S. A. and Caruthers, S. D. (2011). Simultaneous dual-nuclei imaging for motion corrected detection and quantification of 19F imaging agents. Magn. Reson. Med. 66, 1116-1122.
83. Kim, T., Momin, E., Choi, J., Yuan, K., Zaidi, H., Kim, J., Park, M., Lee, N., McMahon, M. T., Quinones-Hinojosa, A. et al. (2011). Mesoporous silica-coated hollow manganese oxide nanoparticles as positive T1 contrast agents for labeling and MRI tracking of adipose-derived mesenchymal stem cells. J. Am. Chem. Soc. 133, 2955-2961.
84. Kodibagkar, V. D., Yu, J., Liu, L., Hetherington, H. P. and Mason, R. P. (2006). Imaging beta-galactosidase activity using 19F chemical shift imaging of LacZ genereporter molecule 2-fluoro-4-nitrophenol-beta-D-galactopyranoside. Magn. Reson. Imaging 24, 959-962.
85. Koretsky, A. P. and Traxler, B. A. (1989). The B isozyme of creatine kinase is active as a fusion protein in Escherichia coli: in vivo detection by 31P NMR. FEBS Lett. 243, 8-12.
86. Koretsky, A. P., and Brosnan, M. J., Chen, L. H., Chen, J. D. and Van Dyke, T. (1990). NMR detection of creatine kinase expressed in liver of transgenic mice: determination of free ADP levels. Proc. Natl. Acad. Sci. USA 87, 3112-3116.
87. Koretsky, A., Lin, Y.-J., Schorle, H. and Jaenisch, R. (1996). Genetic control of MRI contrast by expression of the transferrin receptor. Proc. Int. Soc. Magn. Reson. Med. 4, 69.
88. Kostura, L., and Kraitchman, D. L., Mackay, A. M., Pittenger, M. F. and Bulte, J. W. (2004). Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed. 17, 513-517.
89. Kraitchman, D. L., and Heldman, A. W., Atalar, E., Amado, L. C., and Martin, B. J., Pittenger, M. F., Hare, J. M. and Bulte, J. W. (2003). In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 107, 2290-2293.
90. Krakora, D., Mulcrone, P., Meyer, M., Lewis, C., Bernau, K., Gowing, G., Zimprich, C., Aebischer, P., Svendsen, C. N. and Suzuki, M. (2013). Synergistic effects of GDNF and VEGF on lifespan and disease progression in a familial ALS rat model. Mol. Ther. 21, 1602-1610.
91. Kumar, A., Welti, D. and Ernst, R. R. (1975). NMR Fourier zeugmatography. J. Magn. Reson. 18, 495-509.
92. Lauterbur, P. C. (1973). Image formation by induced local interactions: examples employing nuclear magnetic resonance. Nature 242, 190-191.
93. Lauterbur, P. C. (1974). Magnetic resonance zeugmatography. Pure Appl. Chem. 40, 149-157.
94. Lauterbur, P. C., Mendonca Dias, M. and Rudin, A. M. (1978). Augmentation of tissue water proton spin-lattice relaxation rates by in vivo addition of paramagnetic ions. Electrons to Tissues 1, 752-759.
95. Lebel, R. M., Menon, R. S. and Bowen, C. V. (2006). Relaxometry model of strong dipolar perturbers for balanced-SSFP: application to quantification of SPIO loaded cells. Magn. Reson. Med. 55, 583-591.
96. Lee, T., and Cai, L. X., Lelyveld, V. S., Hai, A. and Jasanoff, A. (2014). Molecular-level functional magnetic resonance imaging of dopaminergic signaling. Science 344, 533-535.
97. Li, W. H., Parigi, G., Fragai, M., Luchinat, C. and Meade, T. J. (2002). Mechanistic studies of a calcium-dependent MRI contrast agent. Inorg. Chem. 41, 4018-4024.
98. Li, C., and Greenwood, T. R., Bhujwalla, Z. M. and Glunde, K. (2006). Synthesis and characterization of glucosamine-bound near-infrared probes for optical imaging. Org. Lett. 8, 3623-3626.
99. Li, Y., Yan, M., Yang, J., Raman, I., Du, Y., Min, S., Fang, X., Mohan, C. and Li, Q. Z. (2014). Glutathione S-transferase Mu 2-transduced mesenchymal stem cells ameliorated anti-glomerular basement membrane antibody-induced glomerulonephritis by inhibiting oxidation and inflammation. Stem Cell Res. Ther. 5, 19.
100. Liang, Y., Ågren, L., Lyczek, A., Walczak, P. and Bulte, J. W. (2013a). Neural progenitor cell survival in mouse brain can be improved by co-transplantation of helper cells expressing bFGF under doxycycline control. Exp. Neurol. 247, 73-79.
101. Liang, Y., Walczak, P. and Bulte, J. W. (2013b). The survival of engrafted neural stem cells within hyaluronic acid hydrogels. Biomaterials 34, 5521-5529.
102. Liang, Y., Bar-Shir, A., Song, X., and Gilad, A. A., Walczak, P. and Bulte, J. W. (2015). Label-free imaging of gelatin-containing hydrogel scaffolds. Biomaterials 42, 144-150.
103. Liu, L., and Kodibagkar, V. D., Yu, J. X. and Mason, R. P. (2007). 19F-NMR detection of lacZ gene expression via the enzymic hydrolysis of 2-fluoro-4-nitrophenyl beta-D-galactopyranoside in vivo in PC3 prostate tumor xenografts in the mouse. FASEB J. 21, 2014-2019.
104. Liu, G., Liang, Y., Bar-Shir, A., Chan, K. W., and Galpoththawela, C. S., Bernard, S. M., Tse, T., Yadav, N. N., Walczak, P., McMahon, M. T. et al. (2011). Monitoring enzyme activity using a diamagnetic chemical exchange saturation transfer magnetic resonance imaging contrast agent. J. Am. Chem. Soc. 133, 16326-16329.
105. Liu, G., Song, X., Chan, K. W. and McMahon, M. T. (2013). Nuts and bolts of chemical exchange saturation transfer MRI. NMR Biomed. 26, 810-828.
106. Livramento, J. B., Tóth, E., Sour, A., Borel, A., Merbach, A. E. and Ruloff, R. (2005). High relaxivity confined to a small molecular space: a metallostar-based, potential MRI contrast agent. Angew. Chem. Int. Ed. Engl. 44, 1480-1484.
107. Louie, A. Y., Hüber, M. M., Ahrens, E. T., Rothbächer, U., Moats, R., and Jacobs, R. E., Fraser, S. E. and Meade, T. J. (2000). In vivo visualization of gene expression using magnetic resonance imaging. Nat. Biotechnol. 18, 321-325.
108. Lovejoy, D. B. and Guillemin, G. J. (2014). The potential for transition metal-mediated neurodegeneration in amyotrophic lateral sclerosis. Front. Aging Neurosci. 6, 173.
109. Lubag, A. J., De Leon-Rodriguez, L. M., Burgess, S. C. and Sherry, A. D. (2011). Noninvasive MRI of β-cell function using a Zn2+-responsive contrast agent. Proc. Natl. Acad. Sci. USA 108, 18400-18405.
110. Madelin, G. and Regatte, R. R. (2013). Biomedical applications of sodium MRI in vivo. J. Magn. Reson. Imaging 38, 511-529.
111. Malemud, C. J. (2006). Matrix metalloproteinases (MMPs) in health and disease: an overview. Front. Biosci. 11, 1696-1701.
112. Matsuo, K., Kamada, R., Mizusawa, K., Imai, H., Takayama, Y., Narazaki, M., Matsuda, T., Takaoka, Y. and Hamachi, I. (2013). Specific detection and imaging of enzyme activity by signal-amplifiable self-assembling (19)F MRI probes. Chemistry 19, 12875-12883.
113. Mattson, M. P. (2007). Calcium and neurodegeneration. Aging Cell 6, 337-350.
114. Mertens, M. E., Hermann, A., Bühren, A., Olde-Damink, L., Möckel, D., Gremse, F., Ehling, J., Kiessling, F. and Lammers, T. (2014). Iron Oxide-labeled Collagen Scaffolds for Non-invasive MR Imaging in Tissue Engineering. Adv. Funct. Mater. 24, 754-762.
115. Mertens, M. E., Koch, S., Schuster, P., Wehner, J., Wu, Z., Gremse, F., Schulz, V., Rongen, L., Wolf, F., Frese, J. et al. (2015). USPIO-labeled textile materials for non-invasive MR imaging of tissue-engineered vascular grafts. Biomaterials 39, 155-163.
116. Modo, M., and Beech, J. S., Meade, T. J., Williams, S. C. and Price, J. (2009). A chronic 1 year assessment of MRI contrast agent-labelled neural stem cell transplants in stroke. Neuroimage 47 Suppl. 2, T133-T142.
117. Moore, A., Josephson, L., Bhorade, R. M., Basilion, J. P. and Weissleder, R. (2001). Human transferrin receptor gene as a marker gene for MR imaging. Radiology 221, 244-250.
118. Narita, K., Kawasaki, F. and Kita, H. (1990). Mn and Mg influxes through Ca channels of motor nerve terminals are prevented by verapamil in frogs. Brain Res. 510, 289-295.
119. Nejadnik, H., and Henning, T. D., Castaneda, R. T., Boddington, S., Taubert, S., Jha, P., Tavri, S., Golovko, D., Ackerman, L., Meier, R. et al. (2012a). Somatic differentiation and MR imaging of magnetically labeled human embryonic stem cells. Cell Transplant. 21, 2555-2567.
120. Nejadnik, H., and Henning, T. D., Do, T., Sutton, E. J., Baehner, F., Horvai, A., Sennino, B., McDonald, D., Meier, R., Misselwitz, B. et al. (2012b). MR imaging features of gadofluorine-labeled matrix-associated stem cell implants in cartilage defects. PLoS ONE 7, e49971.
121. Nkansah, M. K., Thakral, D. and Shapiro, E. M. (2011). Magnetic poly(lactide-coglycolide) and cellulose particles for MRI-based cell tracking. Magn. Reson. Med. 65, 1776-1785.
122. Norman, A. B., and Thomas, S. R., Pratt, R. G., Lu, S. Y. and Norgren, R. B. (1992). Magnetic resonance imaging of neural transplants in rat brain using a superparamagnetic contrast agent. Brain Res. 594, 279-283.
123. Partlow, K. C., Chen, J., Brant, J. A., and Neubauer, A. M., Meyerrose, T. E., Creer, M. H., Nolta, J. A., Caruthers, S. D., Lanza, G. M. and Wickline, S. A. (2007). 19F magnetic resonance imaging for stem/progenitor cell tracking with multiple unique perfluorocarbon nanobeacons. FASEB J. 21, 1647-1654.
124. Patrick, P. S., and Kettunen, M. I., Tee, S. S., Rodrigues, T. B., Serrao, E., and Timm, K. N., McGuire, S. and Brindle, K. M. (2014). Detection of transgene expression using hyperpolarized (13) C urea and diffusion-weighted magnetic resonance spectroscopy. Magn. Reson. Med. [Epub ahead of print] doi: 10.1002/mrm.25254.
125. Perez, J. M., Josephson, L., O'Loughlin, T., Högemann, D. and Weissleder, R. (2002). Magnetic relaxation switches capable of sensing molecular interactions. Nat. Biotechnol. 20, 816-820.
126. Proctor, W. G. and Yu, F. C. (1950). The dependence of a nuclear magnetic resonance frequency upon chemical compound. Phys. Rev. 77, 717.
127. Purcell, E. M., Torrey, H. C. and Pound, R. V. (1946). Resonance absorption by nuclear magnetic moments in a solid. Phys. Rev. 69, 37-38.
128. Que, E. L. and Chang, C. J. (2006). A smart magnetic resonance contrast agent for selective copper sensing. J. Am. Chem. Soc. 128, 15942-15943.
129. Que, E. L. and Chang, C. J. (2010). Responsive magnetic resonance imaging contrast agents as chemical sensors for metals in biology and medicine. Chem. Soc. Rev. 39, 51-60.
130. Que, E. L., New, E. J. and Chang, C. J. (2012). A cell-permeable gadolinium contrast agent for magnetic resonance imaging of copper in a Menkes disease model. Chemical Science 3, 1829-1834.
131. Rad, A. M., and Arbab, A. S., Iskander, A. S., Jiang, Q. and Soltanian-Zadeh, H. (2007). Quantification of superparamagnetic iron oxide (SPIO)-labeled cells using MRI. J. Magn. Reson. Imaging 26, 366-374.
132. Razgulin, A., Ma, N. and Rao, J. (2011). Strategies for in vivo imaging of enzyme activity: an overview and recent advances. Chem. Soc. Rev. 40, 4186-4216.
133. Richards, J. M., and Shaw, C. A., Lang, N. N., Williams, M. C., and Semple, S. I., MacGillivray, T. J., Gray, C., Crawford, J. H., Alam, S. R., Atkinson, A. P. et al. (2012). In vivo mononuclear cell tracking using superparamagnetic particles of iron oxide: feasibility and safety in humans. Circ. Cardiovasc. Imaging 5, 509-517.
134. Robberecht, W. and Philips, T. (2013). The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 14, 248-264.
135. Rodríguez, E., Nilges, M., Weissleder, R. and Chen, J. W. (2010). Activatable magnetic resonance imaging agents for myeloperoxidase sensing: mechanism of activation, stability, and toxicity. J. Am. Chem. Soc. 132, 168-177.
136. Rohani, R., Figueredo, R., Bureau, Y., Koropatnick, J., Foster, P., Thompson, R. T., Prato, F. S. and Goldhawk, D. E. (2014). Imaging tumor growth non-invasively using expression of MagA or modified ferritin subunits to augment intracellular contrast for repetitive MRI. Mol. Imaging Biol. 16, 63-73.
137. Roos, A. and Boron, W. F. (1981). Intracellular pH. Physiol. Rev. 61, 296-434.
138. Rudelius, M., Daldrup-Link, H. E., Heinzmann, U., Piontek, G., Settles, M., Link, T. M. and Schlegel, J. (2003). Highly efficient paramagnetic labelling of embryonic and neuronal stem cells. Eur. J. Nucl. Med. Mol. Imaging 30, 1038-1044.
139. Ruiz-Cabello, J., Walczak, P., and Kedziorek, D. A., Chacko, V. P., Schmieder, A. H., and Wickline, S. A., Lanza, G. M. and Bulte, J. W. (2008). In vivo "hot spot" MR imaging of neural stem cells using fluorinated nanoparticles. Magn. Reson. Med. 60, 1506-1511.
140. Ruiz-Cabello, J., Barnett, B. P., Bottomley, P. A. and Bulte, J. W. (2011). Fluorine (19F) MRS and MRI in biomedicine. NMR Biomed. 24, 114-129.
141. Schellenberger, E., Rudloff, F., Warmuth, C., Taupitz, M., Hamm, B. and Schnorr, J. (2008). Protease-specific nanosensors for magnetic resonance imaging. Bioconjug. Chem. 19, 2440-2445.
142. Schmidt, R., Nippe, N., Strobel, K., Masthoff, M., Reifschneider, O., Castelli, D. D., Höltke, C., Aime, S., Karst, U., Sunderkötter, C. et al. (2014). Highly shifted proton MR imaging: cell tracking by using direct detection of paramagnetic compounds. Radiology 272, 785-795.
143. Shapiro, M. G., and Szablowski, J. O., Langer, R. and Jasanoff, A. (2009). Protein nanoparticles engineered to sense kinase activity in MRI. J. Am. Chem. Soc. 131, 2484-2486.
144. Shapiro, M. G., and Westmeyer, G. G., Romero, P. A., Szablowski, J. O., Küster, B., Shah, A., and Otey, C. R., Langer, R., Arnold, F. H. and Jasanoff, A. (2010). Directed evolution of a magnetic resonance imaging contrast agent for noninvasive imaging of dopamine. Nat. Biotechnol. 28, 264-270.
145. Shapiro, M. G., and Ramirez, R. M., Sperling, L. J., Sun, G., Sun, J., Pines, A., Schaffer, D. V. and Bajaj, V. S. (2014). Genetically encoded reporters for hyperpolarized xenon magnetic resonance imaging. Nat. Chem. 6, 629-634.
146. Sherry, A. D. and Woods, M. (2008). Chemical exchange saturation transfer contrast agents for magnetic resonance imaging. Annu. Rev. Biomed. Eng. 10, 391-411.
147. Silva, A. C. and Bock, N. A. (2008). Manganese-enhanced MRI: an exceptional tool in translational neuroimaging. Schizophr. Bull. 34, 595-604.
148. Srinivas, M., and Morel, P. A., Ernst, L. A., Laidlaw, D. H. and Ahrens, E. T. (2007). Fluorine-19 MRI for visualization and quantification of cell migration in a diabetes model. Magn. Reson. Med. 58, 725-734.
149. Srivastava, A. K. and Bulte, J. W. (2014). Seeing stem cells at work in vivo. Stem Cell Rev. 10, 127-144.
150. Stephenson, E., Nathoo, N., Mahjoub, Y., Dunn, J. F. and Yong, V. W. (2014). Iron in multiple sclerosis: roles in neurodegeneration and repair. Nat. Rev. Neurol. 10, 459-468.
151. Suzuki, M., McHugh, J., Tork, C., Shelley, B., Hayes, A., Bellantuono, I., Aebischer, P. and Svendsen, C. N. (2008). Direct muscle delivery of GDNF with human mesenchymal stem cells improves motor neuron survival and function in a rat model of familial ALS. Mol. Ther. 16, 2002-2010.
152. Tang, K. S. and Shapiro, E. M. (2011). Enhanced magnetic cell labeling efficiency using - NH2 coated MPIOs. Magn. Reson. Med. 65, 1564-1569.
153. Tei, L., Mazooz, G., Shellef, Y., Avni, R., Vandoorne, K., Barge, A., Kalchenko, V., Dewhirst, M. W., Chaabane, L., Miragoli, L. et al. (2010). Novel MRI and fluorescent probes responsive to the Factor XIII transglutaminase activity. Contrast Media Mol. Imaging 5, 213-222.
154. Temme, S., Bönner, F., Schrader, J. and Flögel, U. (2012). 19F magnetic resonance imaging of endogenous macrophages in inflammation. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 4, 329-343.
155. Terrovitis, J., Stuber, M., Youssef, A., Preece, S., Leppo, M., Kizana, E., Schär, M., Gerstenblith, G., Weiss, R. G., Marbán, E. et al. (2008). Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation 117, 1555-1562.
156. Thomas, J. A., and Buchsbaum, R. N., Zimniak, A. and Racker, E. (1979). Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18, 2210-2218.
157. Thomas, D. C., and Wong, F. S., Zaccone, P., Green, E. A. and Wållberg, M. (2013). Protection of islet grafts through transforming growth factor-β-induced tolerogenic dendritic cells. Diabetes 62, 3132-3142.
158. Thomsen, H. S. (2006). Nephrogenic systemic fibrosis: A serious late adverse reaction to gadodiamide. Eur. Radiol. 16, 2619-2621.
159. Tjuvajev, J. G., Stockhammer, G., Desai, R., Uehara, H., Watanabe, K., Gansbacher, B. and Blasberg, R. G. (1995). Imaging the expression of transfected genes in vivo. Cancer Res. 55, 6126-6132.
160. Trokowski, R., Ren, J., Kálmán, F. K. and Sherry, A. D. (2005). Selective sensing of zinc ions with a PARACEST contrast agent. Angew. Chem. Int. Ed. Engl. 44, 6920-6923.
161. Tseng, C. L., and Shih, I. L., Stobinski, L. and Lin, F. H. (2010). Gadolinium hexanedione nanoparticles for stem cell labeling and tracking via magnetic resonance imaging. Biomaterials 31, 5427-5435.
162. Vandsburger, M. H., Radoul, M., Cohen, B. and Neeman, M. (2013). MRI reporter genes: applications for imaging of cell survival, proliferation, migration and differentiation. NMR Biomed. 26, 872-884.
163. Walter, G., Barton, E. R. and Sweeney, H. L. (2000). Noninvasive measurement of gene expression in skeletal muscle. Proc. Natl. Acad. Sci. USA 97, 5151-5155.
164. Wang, Y., Wang, Y., Wang, L., Che, Y., Li, Z. and Kong, D. (2011). Preparation and evaluation of magnetic nanoparticles for cell labeling. J. Nanosci. Nanotechnol. 11, 3749-3756.
165. Ward, K. M. and Balaban, R. S. (2000). Determination of pH using water protons and chemical exchange dependent saturation transfer (CEST). Magn. Reson. Med. 44, 799-802.
166. Weissleder, R., Simonova, M., Bogdanova, A., Bredow, S., Enochs, W. S. and Bogdanov, A., Jr (1997). MR imaging and scintigraphy of gene expression through melanin induction. Radiology 204, 425-429.
167. Weissleder, R., Moore, A., Mahmood, U., Bhorade, R., Benveniste, H., Chiocca, E. A. and Basilion, J. P. (2000). In vivo magnetic resonance imaging of transgene expression. Nat. Med. 6, 351-355.
168. Westmeyer, G. G., Durocher, Y. and Jasanoff, A. (2010). A secreted enzyme reporter system for MRI. Angew. Chem. Int. Ed. Engl. 49, 3909-3911.
169. Westmeyer, G. G., Emer, Y., Lintelmann, J. and Jasanoff, A. (2014). MRI-based detection of alkaline phosphatase gene reporter activity using a porphyrin solubility switch. Chem. Biol. 21, 422-429.
170. Xie, X., Cao, F., Sheikh, A. Y., Li, Z., and Connolly, A. J., Pei, X., Li, R. K., Robbins, R. C. and Wu, J. C. (2007). Genetic modification of embryonic stem cells with VEGF enhances cell survival and improves cardiac function. Cloning Stem Cells 9, 549-563.
171. Yaghoubi, S. S., and Jensen, M. C., Satyamurthy, N., Budhiraja, S., Paik, D., Czernin, J. and Gambhir, S. S. (2009). Noninvasive detection of therapeutic cytolytic T cells with 18F-FHBG PET in a patient with glioma. Nat. Clin. Pract. Oncol. 6, 53-58.
172. Yoo, B. and Pagel, M. D. (2006). A PARACEST MRI contrast agent to detect enzyme activity. J. Am. Chem. Soc. 128, 14032-14033.
173. Yoo, B., and Sheth, V. R., Howison, C. M., Douglas, M. J., and Pineda, C. T., Maine, E. A., Baker, A. F. and Pagel, M. D. (2013). Detection of in vivo enzyme activity with Cataly CEST MRI. Magn. Reson. Med.
174. Yu, J. X., and Kodibagkar, V. D., Hallac, R. R., Liu, L. and Mason, R. P. (2012). Dual 19F/1H MR gene reporter molecules for in vivo detection of β-galactosidase. Bioconjug. Chem. 23, 596-603.
175. Zhang, S., Winter, P., Wu, K. and Sherry, A. D. (2001). A novel europium(III)-based MRI contrast agent. J. Am. Chem. Soc. 123, 1517-1518.
176. Zhang, H., Zhou, L. and Zhang, W. (2014). Control of scaffold degradation in tissue engineering: a review. Tissue Eng. Part B Rev. 20, 492-502.
177. Zhong, J., Sakaki, M., Okada, H. and Ahrens, E. T. (2013). In vivo intracellular oxygen dynamics in murine brain glioma and immunotherapeutic response of cytotoxic T cells observed by fluorine-19 magnetic resonance imaging. PLoS ONE 8, e59479.
178. Ziv, K., Meir, G., Harmelin, A., Shimoni, E., Klein, E. and Neeman, M. (2010). Ferritin as a reporter gene for MRI: chronic liver over expression of H-ferritin during dietary iron supplementation and aging. NMR Biomed. 23, 523-531.
179. Zurkiya, O., Chan, A. W. and Hu, X. (2008). MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Magn. Reson. Med. 59, 1225-1231.