Can magnetic targeting of magnetically labeled circulating cells optimize intramyocardial cell retention?

Cell Transplantation

Volumn 21, Issue 4, 2012, Pages 679-691

  Chaudeurge, Aurélie ^a,b   Wilhelm, Claire ^c,d   Chen Toumoux, Annabel ^a,b   Farahmand, Patrick ^a,d,e   Bellamy, Valérie ^a,b   Autret, Gwennhael ^d,e   Menager, Christine ^g   Hagege, Albert ^a,d,e   Larghero, Jerome ^d,h   Gazeau, Florence ^a,d   Clement, Olivier ^e,f   Menasche, Philippe ^d,e  

^a INSERM   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^f PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^g SORBONNE UNIVERSITÉ   (France)

^h SAINT LOUIS HOSPITAL   (France)

Author keywords

Endothelial progenitor cells (EPCs); Homing; Magnetic targeting; Myocardial infarction

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CITRIC ACID; IRON OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; ARTERY CLAMP; ARTERY OCCLUSION; ARTICLE; CELL HOMING; CELL LABELING; CELL MIGRATION; CELL PROLIFERATION; CELL THERAPY; CONTROLLED STUDY; CORONARY ARTERY; CULTURE MEDIUM; ENDOTHELIAL PROGENITOR CELL; EXPLANT; HEART INFARCTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAGNETISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVOR; THORACIC CAVITY;

ANIMALIA; RATTUS;

EID: 84930483087     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X612440     Document Type: Article

References (43)

1. Aicher, A.; Heeschen, C.; Sasaki, K.; Urbich, C.; Zeiher, A. M.; Dimmeler, S. Low-energy shock wave for enhanc-ing recruitment of endothelial progenitor cells: A new modality to increase efficacy of cell therapy in chronic hind limb ischemia. Circulation 114:2823-2830; 2006.
2. Amsalem, Y.; Mardor, Y.; Feinberg, M. S.; Landa, N.; Miller, L.; Daniels, D.; Ocherashvilli, A.; Holbova, R.; Yosef, O.; Barbash, I. M.; Leor, J. Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium. Circulation 116:I38-45; 2007.
3. Arbab, A. S.; Frank, J. A. Cellular MRI and its role in stem cell therapy. Regen. Med. 3:199-215; 2008.
4. Arbab, A. S.; Jordan, E. K.; Wilson, L. B.; Yocum, G. T.; Lewis, B. K.; Frank, J. A. In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum. Gene Ther. 15:351-360; 2004.
5. Assis, A. C.; Carvalho, J. L.; Jacoby, B. A.; Ferreira, R. L.; Castanheira, P.; Diniz, S. O.; Cardoso, V. N.; Goes, A. M.; Ferreira, A. J. Time-dependent migration of sys-temically delivered bone marrow mesenchymal stem cells to the infarcted heart. Cell Transplant. 19:219-230; 2010.
6. Bulte, J. W.; Kraitchman, D. L. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 17:484-499; 2004.
7. Bulte, J. W.; Kraitchman, D. L. Monitoring cell therapy using iron oxide MR contrast agents. Curr. Pharm. Biotechnol. 5:567-584; 2004.
8. Carr, C. A.; Stuckey, D. J.; Tatton, L.; Tyler, D. J.; Hale, S. J.; Sweeney, D.; Schneider, J. E.; Martin-Rendon, E.; Radda, G. K.; Harding, S. E.; Watt, S. M.; Clarke, K. Bone marrow-derived stromal cells home to and remain in the infarcted rat heart but fail to improve function: An in vivo cine-MRI study. Am. J. Physiol. Heart Circ. Physiol. 295:H533-542; 2008.
9. Chavakis, E.; Aicher, A.; Heeschen, C.; Sasaki, K.; Kaiser, R.; El Makhfi, N.; Urbich, C.; Peters, T.; Scharffetter-Kochanek, K.; Zeiher, A. M.; Chavakis, T.; Dimmeler, S. Role of beta2-integrins for homing and neovascularization capacity of endothelial progenitor cells. J. Exp. Med. 201: 63-72; 2005.
10. Cheng, K.; Li, T. S.; Malliaras, K.; Davis, D. R.; Zhang, Y.; Marban, E. Magnetic targeting enhances engraftment and functional benefit of iron-labeled cardiosphere-derived cells in myocardial infarction. Circ. Res. 106: 1570-1581; 2010.
11. Cheng, Z.; Ou, L.; Zhou, X.; Li, F.; Jia, X.; Zhang, Y.; Liu, X.; Li, Y.; Ward, C. A.; Melo, L. G.; Kong, D. Tar-geted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance. Mol. Ther. 16:571-579; 2008.
12. Forbes, Z. G.; Yellen, B. B.; Halverson, D. S.; Fridman, G.; Barbee, K. A.; Friedman, G. Validation of high gradi-ent magnetic field based drug delivery to magnetizable implants under flow. IEEE Trans. Biomed. Eng. 55:643-649; 2008.
13. Fortin-Ripoche, J. P.; Martina, M. S.; Gazeau, F.; Menager, C.; Wilhelm, C.; Bacri, J. C.; Lesieur, S.; Clement, O. Magnetic targeting of magnetoliposomes to solid tumors with MR imaging monitoring in mice: Feasi-bility. Radiology 239:415-424; 2006.
14. Frasca, G.; Gazeau, F.; Wilhelm, C. Formation of a three-dimensional multicellular assembly using magnetic pat-terning. Langmuir 25:2348-2354; 2009.
15. Fukuhara, S.; Tomita, S.; Nakatani, T.; Ohtsu, Y.; Ishida, M.; Yutani, C.; Kitamura, S. G-CSF promotes bone marrow cells to migrate into infarcted mice heart, and dif-ferentiate into cardiomyocytes. Cell Transplant. 13:741-748; 2004.
16. Ghanem, A.; Steingen, C.; Brenig, F.; Funcke, F.; Bai, Z. Y.; Hall, C.; Chin, C. T.; Nickenig, G.; Bloch, W.; Tiemann, K. Focused ultrasound-induced stimulation of microbubbles augments site-targeted engraftment of mes-enchymal stem cells after acute myocardial infarction. J. Mol. Cell. Cardiol. 47:411-418; 2009.
17. Hansson, E. M.; Lindsay, M. E.; Chien, K. R. Regenera-tion next: Toward heart stem cell therapeutics. Cell Stem Cell 5:364-377; 2009.
18. Hayashi, M.; Li, T. S.; Ito, H.; Mikamo, A.; Hamano, K. Comparison of intramyocardial and intravenous routes of delivering bone marrow cells for the treatment of ischemic heart disease: An experimental study. Cell Transplant. 13: 639-647; 2004.
19. Henning, R. J.; Burgos, J. D.; Vasko, M.; Alvarado, F.; Sanberg, C. D.; Sanberg, P. R.; Morgan, M. B. Human cord blood cells and myocardial infarction: Effect of dose and route of administration on infarct size. Cell Transplant. 16:907-917; 2007.
20. Hofmann, A.; Wenzel, D.; Becher, U. M.; Freitag, D. F.; Klein, A. M.; Eberbeck, D.; Schulte, M.; Zimmermann, K.; Bergemann, C.; Gleich, B.; Roell, W.; Weyh, T.; Trahms, L.; Nickenig, G.; Fleischmann, B. K.; Pfeifer, A. Combined targeting of lentiviral vectors and positioning of transduced cells by magnetic nanoparticles. Proc. Natl. Acad. Sci. USA 106:44-49; 2009.
21. Hofmann, M.; Wollert, K. C.; Meyer, G. P.; Menke, A.; Arseniev, L.; Hertenstein, B.; Ganser, A.; Knapp, W. H.; Drexler, H. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111:2198-2202; 2005.
22. Ito, A.; Takizawa, Y.; Honda, H.; Hata, K.; Kagami, H.; Ueda, M.; Kobayashi, T. Tissue engineering using magne-tite nanoparticles and magnetic force: Heterotypic layers of cocultured hepatocytes and endothelial cells. Tissue Eng. 10:833-840; 2004.
23. Kyrtatos, P. G.; Lehtolainen, P.; Junemann-Ramirez, M.; Garcia-Prieto, A.; Price, A. N.; Martin, J. F.; Gadian, D. G.; Pankhurst, Q. A.; Lythgoe, M. F. Magnetic tagging increases delivery of circulating progenitors in vascular injury. JACC Cardiovasc. Interv. 2:794-802; 2009.
24. Li, W.; Ma, N.; Ong, L. L.; Kaminski, A.; Skrabal, C.; Ugurlucan, M.; Lorenz, P.; Gatzen, H. H.; Lutzow, K.; Lendlein, A.; Putzer, B. M.; Li, R. K.; Steinhoff, G. Enhanced thoracic gene delivery by magnetic nanobead-mediated vector. J. Gene Med. 10:897-909; 2008.
25. Lipinski, M. J.; Biondi-Zoccai, G. G.; Abbate, A.; Khianey, R.; Sheiban, I.; Bartunek, J.; Vanderheyden, M.; Kim, H. S.; Kang, H. J.; Strauer, B. E.; Vetrovec, G. W. Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction: A collaborative systematic review and meta-analysis of controlled clinical trials. J. Am. Coll. Cardiol. 50:1761-1767; 2007.
26. Luciani, A.; Wilhelm, C.; Bruneval, P.; Cunin, P.; Autret, G.; Rahmouni, A.; Clement, O.; Gazeau, F. Magnetic tar-geting of iron-oxide-labeled fluorescent hepatoma cells to the liver. Eur. Radiol. 19:1087-1096; 2009.
27. Lutz, M.; Rosenberg, M.; Kiessling, F.; Eckstein, V.; Heger, T.; Krebs, J.; Ho, A. D.; Katus, H. A.; Frey, N. Local injection of stem cell factor (SCF) improves myo-cardial homing of systemically delivered c-kit + bone marrow-derived stem cells. Cardiovasc. Res. 77:143-150; 2008.
28. Orlic, D.; Kajstura, J.; Chimenti, S.; Jakoniuk, I.; Anderson, S. M.; Li, B.; Pickel, J.; McKay, R.; Nadal-Ginard, B.; Bodine, D. M.; Leri, A.; Anversa, P. Bone marrow cells regenerate infarcted myocardium. Nature 410:701-705; 2001.
29. Pamme, N.; Wilhelm, C. Continuous sorting of magnetic cells via on-chip free-flow magnetophoresis. Lab Chip 6: 974-980; 2006.
30. Pislaru, S. V.; Harbuzariu, A.; Agarwal, G.; Witt, T.; Gulati, R.; Sandhu, N. P.; Mueske, C.; Kalra, M.; Simari, R. D.; Sandhu, G. S. Magnetic forces enable rapid endothelialization of synthetic vascular grafts. Circulation 114:1314-1318; 2006.
31. Pislaru, S. V.; Harbuzariu, A.; Gulati, R.; Witt, T.; Sandhu, N. P.; Simari, R. D.; Sandhu, G. S. Magnetically targeted endothelial cell localization in stented vessels. J. Am. Coll. Cardiol. 48:1839-1845; 2006.
32. Polyak, B.; Fishbein, I.; Chorny, M.; Alferiev, I.; Williams, D.; Yellen, B.; Friedman, G.; Levy, R. J. High field gradient targeting of magnetic nanoparticle-loaded endothelial cells to the surfaces of steel stents. Proc. Natl. Acad. Sci. USA 105:698-703; 2008.
33. Qian, C.; Tio, R. A.; Roks, A. J.; Boddeus, K. M.; Harmsen, M. C.; van Gilst, W. H.; Schoemaker, R. G. A promising technique for transplantation of bone marrow-derived endothelial progenitor cells into rat heart. Cardiovasc. Pathol. 16:127-135; 2007.
34. Riviere, C.; Martina, M. S.; Tomita, Y.; Wilhelm, C.; Tran Dinh, A.; Menager, C.; Pinard, E.; Lesieur, S.; Gazeau, F.; Seylaz, J. Magnetic targeting of nanometric magnetic fluid loaded liposomes to specific brain intravascular areas: A dynamic imaging study in mice. Radiology 244: 439-448; 2007.
35. Sackstein, R.; Merzaban, J. S.; Cain, D. W.; Dagia, N. M.; Spencer, J. A.; Lin, C. P.; Wohlgemuth, R. Ex vivo glycan engineering of CD44 programs human multipotent mesen-chymal stromal cell trafficking to bone. Nat. Med. 14: 181-187; 2008.
36. Saxena, A.; Fish, J. E.; White, M. D.; Yu, S.; Smyth, J. W.; Shaw, R. M.; DiMaio, J. M.; Srivastava, D. Stromal cell-derived factor-1alpha is cardioprotective after myo-cardial infarction. Circulation 117:2224-2231; 2008.
37. So, P. W.; Kalber, T.; Hunt, D.; Farquharson, M.; Al-Ebraheem, A.; Parkes, H. G.; Simon, R.; Bell, J. D. Effi-cient and rapid labeling of transplanted cell populations with superparamagnetic iron oxide nanoparticles using cell surface chemical biotinylation for in vivo monitoring by MRI. Cell Transplant. 19:419-429; 2010.
38. Stuckey, D. J.; Carr, C. A.; Martin-Rendon, E.; Tyler, D. J.; Willmott, C.; Cassidy, P. J.; Hale, S. J.; Schneider, J. E.; Tatton, L.; Harding, S. E.; Radda, G. K.; Watt, S.; Clarke, K. Iron particles for noninvasive monitoring of bone marrow stromal cell engraftment into, and isolation of viable engrafted donor cells from, the heart. Stem Cells 24:1968-1975; 2006.
39. Wang, X.; Jameel, M. N.; Li, Q.; Mansoor, A.; Qiang, X.; Swingen, C.; Panetta, C.; Zhang, J. Stem cells for myocar-dial repair with use of a transarterial catheter. Circulation 120:S238-246; 2009.
40. Wilhelm, C. Out-of-equilibrium microrheology inside liv-ing cells. Phys. Rev. Lett. 101:028101; 2008.
41. Wilhelm, C.; Bal, L.; Smirnov, P.; Galy-Fauroux, I.; Clement, O.; Gazeau, F.; Emmerich, J. Magnetic control of vascular network formation with magnetically labeled endothelial progenitor cells. Biomaterials 28:3797-3806; 2007.
42. Wilhelm, C.; Billotey, C.; Roger, J.; Pons, J. N.; Bacri, J. C.; Gazeau, F. Intracellular uptake of anionic superpara-magnetic nanoparticles as a function of their surface coat-ing. Biomaterials 24:1001-1011; 2003.
43. Wilhelm, C.; Gazeau, F. Universal cell labelling with anionic magnetic nanoparticles. Biomaterials 29:3161-3174; 2008.