CARS microscopy for the visualization of micrometer-sized iron oxide MRI contrast agents in living cells

Biomedical Optics Express

Volumn 2, Issue 9, 2011, Pages 2470-2483

  Rago, Gianluca ^a   Langer, Carolin M ^b   Brackman, Christian ^c   Day, James P R ^a   Domke, Katrin F ^a   Raschzok, Nathanael ^b   Schmidt, Christian ^d   Sauer, Igor M ^b   Enejder, Annika ^c   Mogl, Martina T ^b   Bonn, Mischa ^a  

^a FOM INSTITUTE AMOLF   (Netherlands)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^d Microparticles GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IRON OXIDES; MAGNETIC RESONANCE IMAGING; MICROMETERS; RAMAN SPECTROSCOPY; VISUALIZATION;

CELLULAR COMPONENTS; COHERENT ANTI-STOKES RAMAN SCATTERING MICROSCOPY; CONTRAST AGENT; IN-VIVO; IN-VIVO IMAGING; INTRACELLULAR LOCALIZATION; IRON OXIDE PARTICLES; LABEL FREE; LABELED CELLS; LIVING CELL; MRI CONTRAST AGENTS; PARTICLE UPTAKES; SINGLE-CELL LEVEL; SUBMICRON RESOLUTION; THREE DIMENSIONS;

COHERENT SCATTERING;

EID: 84865614979     PISSN: None     EISSN: 21567085     Source Type: Journal    
DOI: 10.1364/BOE.2.002470     Document Type: Article

References (56)

1. K. Krause, C. Schneider, K. H. Kuck, and K. Jaquet, "Review: Stem cell therapy in cardiovascular disorders, " Cardiovasc. Ther. 28(5), e101-e110 (2010).
2. T. Meyerrose, S. Olson, S. Pontow, S. Kalomoiris, Y. Jung, G. Annett, G. Bauer, and J. A. Nolta, "Mesenchymal stem cells for the sustained in vivo delivery of bioactive factors, " Adv. Drug Deliv. Rev. 62(12), 1167-1174 (2010).
3. J. Meyburg, A. M. Das, F. Hoerster, M. Lindner, H. Kriegbaum, G. Engelmann, J. Schmidt, M. Ott, A. Pettenazzo, T. Luecke, H. Bertram, G. F. Hoffmann, and A. Burlina, "One liver for four children: first clinical series of liver cell transplantation for severe neonatal urea cycle defects, " Transplantation 87(5), 636-641 (2009).
4. A. Dhawan, J. Puppi, R. D. Hughes, and R. R. Mitry, "Human hepatocyte transplantation: current experience and future challenges, " Natl. Rev. 7(5), 288-298 (2010).
5. R. A. Fisher and S. C. Strom, "Human hepatocyte transplantation: worldwide results, " Transplantation 82(4), 441-449 (2006).
6. S. Gupta, "Hepatocyte transplantation, " J. Gastroenterol. Hepatol. 17(s3 Suppl 3), S287-S293 (2002).
7. A. Dhawan, R. R. Mitry, and R. D. Hughes, "Hepatocyte transplantation for liver-based metabolic disorders, " J. Inherit. Metab. Dis. 29(2-3), 431-435 (2006).
8. Y. Kawashita, C. Guha, K. Yamanouchi, Y. Ito, Y. Kamohara, and T. Kanematsu, "Liver repopulation: a new concept of hepatocyte transplantation, " Surg. Today 35(9), 705-710 (2005).
9. E. Fitzpatrick, R. R. Mitry, and A. Dhawan, "Human hepatocyte transplantation: state of the art, " J. Intern. Med. 266(4), 339-357 (2009).
10. J. W. M. Bulte, "In vivo MRI cell tracking: clinical studies, " AJR Am. J. Roentgenol. 193(2), 314-325 (2009).
11. M. Modo, "Noninvasive imaging of transplanted cells, " Curr. Opin. Organ Transplant. 13(6), 654-658 (2008).
12. J. Puppi and M. Modo, "Use of magnetic resonance imaging contrast agents to detect transplanted liver cells, " Top. Magn. Reson. Imaging 20(2), 113-120 (2009).
13. A. Quaglia, S. C. Lehec, R. D. Hughes, R. R. Mitry, A. S. Knisely, S. Devereaux, J. Richards, M. Rela, N. D. Heaton, B. C. Portmann, and A. Dhawan, "Liver after hepatocyte transplantation for liver-based metabolic disorders in children, " Cell Transplant. 17(12), 1403-1414 (2008).
14. N. I. Bohnen, M. Charron, J. Reyes, W. Rubinstein, S. C. Strom, D. Swanson, and R. Towbin, "Use of indium-111-labeled hepatocytes to determine the biodistribution of transplanted hepatocytes through portal vein infusion, " Clin. Nucl. Med. 25(6), 447-450 (2000).
15. S. Koenig, P. Krause, A. S. A. Hosseini, C. Dullin, M. Rave-Fraenk, S. Kimmina, A. L. Entwistle, R. M. Hermann, C. F. Hess, H. Becker, and H. Christiansen, "Noninvasive imaging of liver repopulation following hepatocyte transplantation, " Cell Transplant. 18(1), 69-78 (2009).
16. W. M. Leevy, S. T. Gammon, J. R. Johnson, A. J. Lampkins, H. Jiang, M. Marquez, D. Piwnica-Worms, M. A. Suckow, and B. D. Smith, "Noninvasive optical imaging of staphylococcus aureus bacterial infection in living mice using a Bis-dipicolylamine-Zinc(II) affinity group conjugated to a near-infrared fluorophore, " Bioconjug. Chem. 19(3), 686-692 (2008).
17. P. F. Renshaw, C. S. Owen, A. E. Evans, and J. S. Leigh, Jr., "Immunospecific NMR contrast agents, " Magn. Reson. Imaging 4(4), 351-357 (1986).
18. S. J. Dodd, M. Williams, J. P. Suhan, D. S. Williams, A. P. Koretsky, and C. Ho, "Detection of single mammalian cells by high-resolution magnetic resonance imaging, " Biophys. J. 76(1), 103-109 (1999).
19. E. M. Shapiro, S. Skrtic, K. Sharer, J. M. Hill, C. E. Dunbar, and A. P. Koretsky, "MRI detection of single particles for cellular imaging, " Proc. Natl. Acad. Sci. U.S.A. 101(30), 10901-10906 (2004).
20. A. S. Arbab and J. A. Frank, "Cellular MRI and its role in stem cell therapy, " Regen. Med. 3(2), 199-215 (2008).
21. E. M. Shapiro, K. Sharer, S. Skrtic, and A. P. Koretsky, "In vivo detection of single cells by MRI, " Magn. Reson. Med. 55(2), 242-249 (2006).
22. J. Grimm, M. F. Kircher, and R. Weissleder, "Cell tracking, " Radiologe 47(1), 25-33 (2007).
23. S. G. Crich, L. Biancone, V. Cantaluppi, D. Duò, G. Esposito, S. Russo, G. Camussi, and S. Aime, "Improved route for the visualization of stem cells labeled with a Gd-/Eu-chelate as dual (MRI and fluorescence) agent, " Magn. Reson. Med. 51(5), 938-944 (2004).
24. H. E. Daldrup-Link, M. Rudelius, S. Metz, G. Piontek, B. Pichler, M. Settles, U. Heinzmann, J. Schlegel, R. A. J. Oostendorp, and E. J. Rummeny, "Cell tracking with gadophrin-2: a bifunctional contrast agent for MR imaging, optical imaging, and fluorescence microscopy, " Eur. J. Nucl. Med. Mol. Imaging 31(9), 1312-1321 (2004).
25. T. D. Henning, O. Saborowski, D. Golovko, S. Boddington, J. S. Bauer, Y. J. Fu, R. Meier, H. Pietsch, B. Sennino, D. M. McDonald, and H. E. Daldrup-Link, "Cell labeling with the positive MR contrast agent Gadofluorine M, " Eur. Radiol. 17(5), 1226-1234 (2007).
26. M. Srinivas, P. A. Morel, L. A. Ernst, D. H. Laidlaw, and E. T. Ahrens, "Fluorine-19 MRI for visualization and quantification of cell migration in a diabetes model, " Magn. Reson. Med. 58(4), 725-734 (2007).
27. N. Himes, J. Y. Min, R. Lee, C. Brown, J. Shea, X. L. Huang, Y. F. Xiao, J. P. Morgan, D. Burstein, and P. Oettgen, "In vivo MRI of embryonic stem cells in a mouse model of myocardial infarction, " Magn. Reson. Med. 52(5), 1214-1219 (2004).
28. J. Pinkernelle, U. Teichgräber, F. Neumann, L. Lehmkuhl, J. Ricke, R. Scholz, A. Jordan, and H. Bruhn, "Imaging of single human carcinoma cells in vitro using a clinical whole-body magnetic resonance scanner at 3.0 T, " Magn. Reson. Med. 53(5), 1187-1192 (2005).
29. J. Lodhia, G. Mandarano, Nj. Ferris, P. Eu, and S. F. Cowell, "Development and use of iron oxide nanoparticles (Part 1): Synthesis of iron oxide nanoparticles for MRI, " Biomed Imaging Intervent. J. 6(2), e12 (2010).
30. M. H. Morgul, N. Raschzok, R. Schwartlander, F. W. Vondran, R. Michel, L. Stelter, J. Pinkernelle, A. Jordan, U. Teichgraber, and I. M. Sauer, "Tracking of primary human hepatocytes with clinical MRI: initial results with Tat-peptide modified superparamagnetic iron oxide particles, " Int. J. Artif. Organs 31(3), 252-257 (2008).
31. W. Liu and J. A. Frank, "Detection and quantification of magnetically labeled cells by cellular MRI, " Eur. J. Radiol. 70(2), 258-264 (2009).
32. I. J. M. de Vries, W. J. Lesterhuis, J. O. Barentsz, P. Verdijk, J. H. van Krieken, O. C. Boerman, W. J. G. Oyen, J. J. Bonenkamp, J. B. Boezeman, G. J. Adema, J. W. M. Bulte, T. W. J. Scheenen, C. J. A. Punt, A. Heerschap, and C. G. Figdor, "Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy, " Nat. Biotechnol. 23(11), 1407-1413 (2005).
33. Z. Medarova, P. Vallabhajosyula, A. Tena, N. Evgenov, P. Pantazopoulos, V. Tchipashvili, G. Weir, D. Sachs, and A. Moore, "In vivo imaging of autologous islet grafts in the liver and under the kidney capsule in non-human primates, " Transplantation 87(11), 1659-1666 (2009).
34. K. A. Hinds, J. M. Hill, E. M. Shapiro, M. O. Laukkanen, A. C. Silva, C. A. Combs, T. R. Varney, R. S. Balaban, A. P. Koretsky, and C. E. Dunbar, "Highly efficient endosomal labeling of progenitor and stem cells with large magnetic particles allows magnetic resonance imaging of single cells, " Blood 102(3), 867-872 (2003).
35. E. M. Shapiro, S. Skrtic, and A. P. Koretsky, "Sizing it up: cellular MRI using micron-sized iron oxide particles, " Magn. Reson. Med. 53(2), 329-338 (2005).
36. N. Raschzok, M. H. Morgul, J. Pinkernelle, F. W. R. Vondran, N. Billecke, N. N. Kammer, G. Pless, M. K. Adonopoulou, C. Leist, L. Stelter, U. Teichgraber, R. Schwartlander, and I. M. Sauer, "Imaging of primary human hepatocytes performed with micron-sized iron oxide particles and clinical magnetic resonance tomography, " J. Cell. Mol. Med. 12(4), 1384-1394 (2008).
37. M. Muller, Introduction to confocal fluorescence microscopy (Shaker Publishing, Maastricht, 2002).
38. S. Schwarz, F. Fernandes, L. Sanroman, M. Hodenius, C. Lang, U. Himmelreich, T. Schmitz-Rode, D. Schueler, M. Hoehn, M. Zenke, and T. Hieronymus, "Synthetic and biogenic magnetite nanoparticles for tracking of stem cells and dendritic cells, " J. Magn. Magn. Mater. 321(10), 1533-1538 (2009).
39. A. M. Schrand, J. J. Schlager, L. M. Dai, and S. M. Hussain, "Preparation of cells for assessing ultrastructural localization of nanoparticles with transmission electron microscopy, " Nat. Protoc. 5(4), 744-757 (2010).
40. J. X. Cheng, A. Volkmer, and X. S. Xie, "Theoretical and experimental characterization of coherent anti-Stokes Raman scattering microscopy, " J. Opt. Soc. Am. B 19(6), 1363-1375 (2002).
41. J. P. R. Day, K. F. Domke, G. Rago, H. Kano, H. O. Hamaguchi, E. M. Vartiainen, and M. Bonn, "Quantitative Coherent Anti-Stokes Raman Scattering (CARS) Microscopy, " J. Phys. Chem. B 115(24), 7713-7725 (2011).
42. A. Enejder, C. Brackmann, and F. Svedberg, "Coherent Anti-Stokes Raman Scattering Microscopy of Cellular Lipid Storage, " IEEE J. Sel. Top. Quantum Electron. 16(3), 506-515 (2010).
43. T. Hashimoto, T. Yamada, and T. Yoko, "Third-order nonlinear optical properties of sol-gel derived alpha-Fe2O3, gamma-Fe2O3, and Fe3O4 thin films, " J. Appl. Phys. 80(6), 3184-3190 (1996).
44. H. S. Nalwa and S. Miyata, Nonlinear Optics of Organic Molecules and Polymers (CRC Press, Boca Raton, FL, 1997).
45. T. Hellerer, C. Axäng, C. Brackmann, P. Hillertz, M. Pilon, and A. Enejder, "Monitoring of lipid storage in Caenorhabditis elegans using coherent anti-Stokes Raman scattering (CARS) microscopy, " Proc. Natl. Acad. Sci. U.S.A. 104(37), 14658-14663 (2007).
46. J. P. R. Day, G. Rago, K. F. Domke, K. P. Velikov, and M. Bonn, "Label-free imaging of lipophilic bioactive molecules during lipid digestion by multiplex coherent anti-Stokes Raman scattering microspectroscopy, " J. Am. Chem. Soc. 132(24), 8433-8439 (2010).
47. M. Okuno, H. Kano, P. Leproux, V. Couderc, J. P. R. Day, M. Bonn, and H. O. Hamaguchi, "Quantitative CARS molecular fingerprinting of single living cells with the use of the maximum entropy method, " Angew. Chem. Int. Ed. Engl. 49(38), 6773-6777 (2010).
48. G. Rago, B. Bauer, F. Svedberg, L. Gunnarsson, M. B. Ericson, M. Bonn, and A. Enejder, "Uptake of gold nanoparticles in healthy and tumor cells visualized by nonlinear optical microscopy, " J. Phys. Chem. B 115(17), 5008-5016 (2011).
49. J. Moger, B. D. Johnston, and C. R. Tyler, "Imaging metal oxide nanoparticles in biological structures with CARS microscopy, " Opt. Express 16(5), 3408-3419 (2008).
50. Y. Zheng, G. Holtom, and S. D. Colson, "Multichannel multiphoton imaging of metal oxides nanoparticles in biological system, " Proc. SPIE 5323, 390-399 (2004).
51. Y. Wang, C.-Y. Lin, A. Nikolaenko, V. Raghunathan, and E. O. Potma, "Four-wave mixing microscopy of nanostructures, " Adv. Opt. Photonics 3(1), 1-52 (2011).
52. J. Burris and T. J. McIlrath, "Theoretical study relating the two-photon absorption cross section to the susceptibility controlling four-wave mixing, " J. Opt. Soc. Am. B 2(8), 1313-1317 (1985).
53. E. W. Van Stryland, M. A. Woodall, H. Vanherzeele, and M. J. Soileau, "Energy band-gap dependence of twophoton absorption, " Opt. Lett. 10(10), 490-492 (1985).
54. J. X. Cheng and X. S. Xie, "Coherent anti-Stokes Raman scattering microscopy: Instrumentation, theory, and applications, " J. Phys. Chem. B 108(3), 827-840 (2004).
55. X. L. Nan, J. X. Cheng, and X. S. Xie, "Vibrational imaging of lipid droplets in live fibroblast cells with coherent anti-Stokes Raman scattering microscopy, " J. Lipid Res. 44(11), 2202-2208 (2003).
56. D. Gachet, F. Billard, N. Sandeau, and H. Rigneault, "Coherent anti-Stokes Raman scattering (CARS) microscopy imaging at interfaces: evidence of interference effects, " Opt. Express 15(16), 10408-10420 (2007).