Long-term in vivo magnetic resonance imaging tracking of endothelial progenitor cells transplanted in rat ischemic limbs and their angiogenic potential

Tissue Engineering - Part A

Volumn 17, Issue 15-16, 2011, Pages 2079-2089

  Agudelo, Carlos A ^a   Tachibana, Yoichi ^a   Noboru, Teramoto ^a   Iida, Hidehiro ^a   Yamaoka, Tetsuji ^a,b  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORINE COMPOUNDS; CYTOLOGY; DEXTRAN; ENDOTHELIAL CELLS; GADOLINIUM; RATS; RESONANCE; STEM CELLS; TISSUE;

BONE MARROW; CELL MIGRATION; CHLORIDE SOLUTIONS; CONTRAST AGENT; ELECTROPORATION; ENDOTHELIAL PROGENITOR CELLS; FLUORESCEIN ISOTHIOCYANATE; HYDROXYL GROUPS; IN-VITRO; IN-VIVO; INTRACELLULAR STABILITY; ISCHEMIC LIMBS; ISCHEMIC TISSUES; LONG DURATION; MAGNETIC RESONANCE IMAGING CONTRAST AGENTS; MODIFIED POLYMER; MR IMAGES; MR SIGNALS; MYOCARDIAL INFARCTION; RAT MODEL; STEM CELL MODEL; STEM CELL THERAPY;

MAGNETIC RESONANCE IMAGING;

RATTUS;

CONTRAST MEDIUM; DEXTRAN; GADOLINIUM 1,4,7,10-TETRAAZACYCLODODECANE-N,N',N'',N'''-TETRAACETATE; GADOTERIC ACID; HETEROCYCLIC COMPOUND; LACTATE DEHYDROGENASE; ORGANOMETALLIC COMPOUND;

ANGIOGENESIS; ANIMAL; ARTICLE; CELL SEPARATION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; ENDOTHELIUM CELL; ENZYMOLOGY; FISCHER 344 RAT; IMMUNOHISTOCHEMISTRY; ISCHEMIA; LIMB; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHENOTYPE; RAT; STAINING; STEM CELL; STEM CELL TRANSPLANTATION; SYNTHESIS; TIME; VASCULARIZATION;

ANIMALS; CELL SEPARATION; CELL SURVIVAL; CONTRAST MEDIA; DEXTRANS; ENDOTHELIAL CELLS; EXTREMITIES; HETEROCYCLIC COMPOUNDS; IMMUNOHISTOCHEMISTRY; ISCHEMIA; L-LACTATE DEHYDROGENASE; MAGNETIC RESONANCE IMAGING; NEOVASCULARIZATION, PHYSIOLOGIC; ORGANOMETALLIC COMPOUNDS; PHENOTYPE; RATS; RATS, INBRED F344; STAINING AND LABELING; STEM CELL TRANSPLANTATION; STEM CELLS; TIME FACTORS;

EID: 79960761986     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2010.0482     Document Type: Article

References (48)

1. Rafii, S., Meeus, S., Dias, S., Hattori, K., Heissig, B., Shemelkov, S., Rafii, D., and Lyden, D. Contribution of morrowderived progenitors to vascular and cardiac regeneration. Cell Devl Biol 13, 61, 2002.
2. Li, Z., Wu, J.C., Sheikh, A.Y., Kraft, D., Cao, F., Xie, X., Patel, M., Gambhir, S.S., Robbins, R.C., Cooke, J.P., and Wu, J.C. Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation 116, I-46, 2007.
3. Kondo, K., Shintani, S., Shibata, R., Murakami, H., Murakami, R., Imaizumi, M., Kitagawa, Y., and Murohara, T. Implantation of adipose-derived regenerative cell enhances ischemia induced angiogenesis. Arterioscler Thromb Vasc B29, 61, 2009.
4. Murohara T. Autologous adipose tissue as a new source of progenitor cells for therapeutic angiogenesis. J Cardiol 53, 155, 2009.
5. Cho, S.W., Moon, S.H., Lee, S.H., Kang, S.W., Kim, J., Lim, J.M., Kim, B.S., and Chung, H.H. Improvement of postnatal neovascularization by embryonic stem cell derived endothelial-like cell transplantation in a mouse model of hindlimb ischemia. Circulation 116, 2409, 2007.
6. Shyu, W.C., Lin, S.Z., Yang, H.I., Tzeng, Y.S., Pang, C.Y., Yen, P.S., and Li, H. Functional recovery of stroke rats induced by granulocyte colony stimulating factor stimulated cells. Circulation 110, 1847, 2004.
7. Urbich, C., and Dimmeler, S. Endothelial progenitor cells characterization and role in vascular biology. Circ Res 95, 343, 2004.
8. Urbich, C., Heesechen, C., Aicher, A., Dernbach, E., Zeiher, A.M., and Dimmeler, S. Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation 108, 2511, 2003.
9. Rafii, S., and Lyden, D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9, 702, 2003.
10. Lewin, M., Carlesso, N., Tung, C.H., Tang, T.X., Cory, D., Scadden, D.T. and Weissleder, R. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat Biotechnol 18, 410, 2000.
11. Hinds, K.A., Hill, J.M., Shapiro, E.M., Laukkanen, M.O., Silva, A.C., Combs, C.A., Varney, T.R., Balaban, R.S., Korestsky, A.P., and Dunbar, C.E. Highly efficient endosomal labeling of progenitor and stem cells with large magnetic particles allows magnetic resonance imaging of single cells. Blood 102, 867, 2003.
12. Bulte, J.W.M., Douglas, T., Witwer, B., Zhang, S.C., Strable, E., Lewis, B.K., Zywicke, H., Miller, B., Gelderen, P.V., Moskowitz, H., Duncan, I.D., and Frank, J.A. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol 19, 1141, 2001.
13. Cormode, D.P., Skajaa T., Fayad, Z.A., and Mulder, W.J.M. Nanotechnology in medical imaging probe design and applications. Arterioscler Thromb Vasc Biol 29, 1, 2009.
14. Wilhelm, C., Bal, L., Smirnov, V., Galy-Fauroux, I., Clement, O., Gazeau, F. and Emmerich, J. Magnetic control of vascular network formation with magnetically labeled endothelial progenitor cells. Biomaterials 28, 3797, 2007.
15. Daldrup-Link, H.E., Rudelius, M., Piontek, G., Metz, S., Brauer, R., Debus, G., Corot, C., Schlegel, J., Link, T.M., Peschel, C., Rummeny, E., and Oostendorp, R.A. Migration of iron oxide-labeled human hematopoietic progenitor cells in a mouse model: in vivo monitoring with 1.5-T MR imaging equipment. Radiology 234, 197, 2005.
16. Arbab A.S., Frenkel, V., Pandit, S.D., Anderson, S.A., Yocum, G.T., Bur, M., Khuu, H.M., Read, E., and Frank, J.A. Magnetic resonance imaging and confocal microscopy studies of magnetically labeled endotelial progenitor cells tracfficking to sites of tumor angiogenesis. Stem Cells 24, 671, 2006.
17. Tachibana, Y., Enmi, J.I., Mahara, A., Iida, H., and Yamaoka, T. Design and characterization of a polymeric MRI contrast agent based on PVA for in vivo living-cell tracking. Contrast Media Mol Imaging 5, 1, 2010.
18. Asahara, T., Murohara, T., Sullivan, A., Silver, M., Zee, R.V.D., Li, T., Witzenbichler, B., Schatteman, G., and Isner, J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science 274, 964, 1997.
19. Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., Kearne, M., Magner, M., and Isner, J.M. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85, 221, 1999.
20. Shi, Q., Rafii, S., Wu, M.H.D., Wijelath, E.S., Yu, C., Ishida, A., Fujita, Y., Kothari, S., Mohle, R., Sauvage, L.R., Moore,M.A.S., Storb, R.F., andHammond, W.P. Evidence for circulating bone marrow-derived endothelial cells. Blood 92, 362, 1998.
21. Kalka, C., Masuda, H., Takahashi, T., Gordon, R., Tepper, O., Gravereaux, E., Pieczek, A., Iwaguro, H., Hayashi, S.I., Isner, J.M., and Asahara, T. Vascular endothelial growth factor165 gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res 86, 1198, 2000.
22. Iwaguro, H., Yamaguchi, J.I., Kalka, C., Murasawa, S., Masuda, H., Hayashi, S.I., Silver, M., Li, T., Isner, J.M., and Asahara, T. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 105, 732, 2002.
23. Lyden, D., Hattori, K., Dias, S., Costa, C., Blaikie, P., Butros, L., Chadburn, A., Heissig, B., Marks, W., Witte, L., Wu, Y., Hicklin, D., Zhu, Z., Hackett, N.R., Crystal, R.G., Moore, M.A.S., Hajjar, K.A., Manova, K., Benezra, R., and Rafii, S. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7, 1194, 2001.
24. Kalka, C., Masuda, H., Takahashi, T., Kalka-Moll, W.M., Silver, M., Kearney, M., LI, T., Isner, J.M., and Asahara, T. Transplantation of ex vivo explanted endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA 28, 3422, 2000.
25. Shintani, S., Murohara, T., Ikeda, H., Ueno, T., Sasaki, K., Duan, J., and Imaizumi, T. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation 103, 897, 2001.
26. Cormode, D.P., Skajaa T., Fayad, Z.A., and Mulder, W.J.M. Nanotechnology in medical imaging probe design and applications. Arterioscler Thromb Vasc Biol 29, 1, 2009.
27. Kamaly, N., Kalber, T., Ahmad, A., Oliver, M.H., So, P.W., Herlihy, A.H., Bell, J.D., Jorgensen, M.R. and Miller, A.D. Bimodal paramagnetic and fluorescent liposomes for cellular and tumor magnetic resonance imaging. Bioconjug Chem 19, 118, 2008.
28. Takahashi, T., Kalka, C., Masuda, H., Chen, D., Silver, M., Kearney, M., Magner, M., Isner, J.M., and Asahara, T. Ischemia-and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5, 434, 1999.
29. Murasawa, S., and Asahara, T. Endothelial progenitor cells for vasculogenesis. Physiology 20, 36, 2005.
30. Kahler, C.M., Wechselberger, J., Hilbe, W., Gschwendtner, A., Colleselli, D., Niederegger, H., Boneberg, E.M., Spizzo, G., Wendel, A., Gunsilius, E., Patsch, J.R., and Hamacher, J. Peripheral infusion of rat bone marrow derived endothelial progenitor cells leads to homing in acute lung injury. J Respir Res 50, 1465, 2007.
31. Kobayashi, N., Fukushima, H., Takeshima, H., Koguchi, W., Mamada, Y., Hirata, H., Machida, Y., Suzuki, N., Yotsuka, F., Tabei, K., Kobayashi, E., Fukuda, N., and Ishimitsu, T. Am J Hypertens 23, 1007, 2010.
32. Iwaguro, H., Yamaguchi, J.I., Kalka, C., Murasawa, S., Masuda, H., Hayashi, S.I., Silver, M., Li, T., Isner, J.M., and Asahara, T. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 105, 732, 2002.
33. Ziada, A.M.A.R., Hudlicka, O., Tyler, K.R., and Wright, A.J.A. The effect of long-term vasodilatation on capillary growth and performance in rabbit heart and skeletal muscle. Cardiovasc Res 18, 724, 1984.
34. Takeshita, S., Isshiki, T., Mori, H., Tanaka, E., Eto, K., Miyazawa, Y., Tanaka, A., Shinozaki, Y., Hyodo, K., Ando, M., Kubota, M., Tanioka, K., Umetani, K., Ochiai, M., Sato, T., and Miyashita, H. Use of synchrotron radiation microangiography to assess development of small collateral arteries in a rat model of hindlimb ischemia. Circulation 95, 805, 1997.
35. Yamaoka, T., Tabata, Y., and Ikada, Y. Body distribution of polysaccharides after intravenous administration. Drug Deliv 1, 75, 1993.
36. Rebizak, R., Schaefer, M., and Dellacherie, E. Polymeric conjugates of Gd3 +-diethylenetriaminepentaacetic acid and dextran 1. Synthesis, characterization, and paramagnetic properties. Bioconjug Chem 8, 605, 1997.
37. De Leon-Rodriguez, L.M., and Kovacs, Z. The synthesis and chelation chemistry of DOTA-peptide conjugates. Bioconjug Chem 19, 391, 2008.
38. Ladd, D.L., Hollister, R., Peng, X., Wei, D., Wu, G., Delecki, D., Snow, R.A., Toner, J.L. Kellar, K., Eck, J., Desai, V.C., Raymond, G., Kinter, L.B., Desser T.S., and Rubien, D.L. Polymeric gadolinium chelate margetic resonance imaging contrast agents: design, synthesis, and properties. Bioconjug Chem 10, 361, 1999.
39. Partlow, K.C., Chen, J., Brant, A., Neubauer, A.M., Meyerrose, T.E., Creer, M.H., Caruthers, S.D., Lanza, G.M., and Wickline, S.A. 19F magnetic resonance imaging for stem/progenitor cell tracking with multiple unique perfluorocarbon nanobeacons. FASEB J 21, 1647, 2007.
40. Amsalem, Y., Mardor, Y., Feinbeg, M.S., Landa, N., Miller, L., Daniels, D., Ocherashvilli, A., Holbova, R., Yosef, O., Barbash, I.M., and Leor, J. Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infracted myocardium. Circulation 116, 38, 2007.
41. Raynal, I., Prigent, P., Peyramaure, S., Najid, A., Rebuzzi, C., and Corot, C. Macrophage endocytosis of superparamagnetic iron oxide nanoparticles. Invest Radiol 39, 56, 2004.
42. Qiao, H., Zhang, H., Zheng, Y., Ponde, D.E., Shen, D., Gao, F., Bakken, A.B., Schmitz, A., Kung, H.F., Ferrari, V.A., and Zhou, R. Embryonic stem cells grafting in normal and infracted myocardium: serial assessment with MR imaging and PET dual detection. Radiology 3, 821, 2009.
43. Srinivasachari, S., Fichter, K.M., and Reineke, T.M., Polycationic b-cyclodestrin "click busters": monodisperse and versatile scaffolds for nucleic acid delivery. J Am Chem Soc 130, 4618, 2008.
44. Mohs, A.M., Wang, X., Goodrich, K.G., Zong, Y., Parker, D.L., and Lu, Z.R. PEG-g-poly(GdDTPA-co-L-cystine): a biodegradable macromolecular blood pool contrast agent for MR imaging. Bioconjug Chem 15, 1424, 2004.
45. Hur, J., Yoon, C.H., Kim, H.S., Choi, J.H., Kang, H.J., Hwang, K.K., Oh, B.H., Lee, M.M., and Park, Y.B. Characterization of two types of endothelial progenitor cells and their different contribution to neovasculogenesis. Arterioscler Thromb Vasc Biol 24, 288, 2004.
46. Gill, M., Dias, S., Hattori, K., Rivera, M.L., Hicklin, D., Witte, L., Girardi, L., Yurt, R., Himel, H., and Raffi, S. Vascular trauma induces rapid but transient mobilization of VEGFR2+ AC133+ endothelial precursor cells. Circ Res 88, 167, 2001.
47. Nissen, N.N., PolverinI, P.J., Koch, A.E., Volin, M.V., Gamelli, R.L., and DiPietro, L.A. Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am J Pathol 152, 1445, 1998.
48. Yamaguchi, J., Kusano, K.F., Masuo, O., Kawamoto, A., Silver, M., Murasawa, S., Bosch-Marce, M., Masuda, H., Losordo, D.W., Isner, J.M., and Asahara, T. Stromal cellderived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107, 1322, 2003.