Focused ultrasound-induced stimulation of microbubbles augments site-targeted engraftment of mesenchymal stem cells after acute myocardial infarction

Journal of Molecular and Cellular Cardiology

Volumn 47, Issue 3, 2009, Pages 411-418

  Ghanem, Alexander ^a   Steingen, Caroline ^b   Brenig, Florian ^b   Funcke, Fabienne ^b   Bai, Zhi Yong ^d   Hall, Christopher ^c   Chin, Chien Ting ^c   Nickenig, Georg ^a   Bloch, Wilhelm ^b   Tiemann, Klaus ^d  

^a UNIVERSITY OF BONN   (Germany)

^b GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

^c PHILIPS RESEARCH LABORATORIES   (Netherlands)

^d UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

Cell therapy; Mesenchymal stem cells; Targeting; Transplantation; Ultrasound

Indexed keywords

PROTEINASE;

ACUTE HEART INFARCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL INVASION; CELL MIGRATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENGRAFTMENT; ENZYME ACTIVITY; HIGH INTENSITY FOCUSED ULTRASOUND; IN VIVO STUDY; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROBUBBLE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CYTOKINES; FEMALE; HEART; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICROBUBBLES; MICROSCOPY, CONFOCAL; MYOCARDIAL INFARCTION; MYOCARDIUM; RATS; RATS, WISTAR; REPERFUSION INJURY; ULTRASONOGRAPHY;

RATTUS;

EID: 67650735147     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.06.008     Document Type: Article

References (26)

1. Assmus B., Schachinger V., Teupe C., Britten M., Lehmann R., Dobert N., et al. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation 106 (2002) 3009-3017
2. Gnecchi M., He H., Liang O.D., Melo L.G., Morello F., Mu H., et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med. 11 (2005) 367-368
3. Barbash I.M., Chouraqui P., Baron J., Feinberg M.S., Etzion S., Tessone A., et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 108 (2003) 863-868
4. Hofmann M., Wollert K.C., Meyer G.P., Menke A., Arseniev L., Hertenstein B., et al. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111 (2005) 2198-2202
5. Schmidt A., Ladage D., Steingen C., Brixius K., Schinkothe T., Klinz F.J., et al. Mesenchymal stem cells transmigrate over the endothelial barrier. Eur. J. Cell Biol. 85 (2006) 1179-1188
6. Steingen C., Brenig F., Baumgartner L., Schmidt J., Schmidt A., and Bloch W. Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J. Mol. Cell. Cardiol. 44 (2008) 1072-1084
7. Chavakis E., Urbich C., and Dimmeler S. Homing and engraftment of progenitor cells: a prerequisite for cell therapy. J. Mol. Cell. Cardiol. 45 (2008) 514-522
8. Song J., Qi M., Kaul S., and Price R.J. Stimulation of arteriogenesis in skeletal muscle by microbubble destruction with ultrasound. Circulation 106 (2002) 1550-1555
9. Imada T., Tatsumi T., Mori Y., Nishiue T., Yoshida M., Masaki H., et al. Targeted delivery of bone marrow mononuclear cells by ultrasound destruction of microbubbles induces both angiogenesis and arteriogenesis response. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 2128-2134
10. Zen K., Okigaki M., Hosokawa Y., Adachi Y., Nozawa Y., Takamiya M., et al. Myocardium-targeted delivery of endothelial progenitor cells by ultrasound-mediated microbubble destruction improves cardiac function via an angiogenic response. J. Mol. Cell. Cardiol. 40 (2006) 799-809
11. Lohmaier S., Ghanem A., Veltmann C., Sommer T., Bruce M., and Tiemann K. In vitro and in vivo studies on continuous echo-contrast application strategies using SonoVue in a newly developed rotating pump setup. Ultrasound Med. Biol. 30 (2004) 1145-1151
12. Nossuli T.O., Lakshminarayanan V., Baumgarten G., Taffet G.E., Ballantyne C.M., Michael L.H., et al. A chronic mouse model of myocardial ischemia-reperfusion: essential in cytokine studies. Am. J. Physiol, Heart Circ. Physiol. 278 (2000) H1049-H1055
13. Kim S.C., Ghanem A., Stapel H., Tiemann K., Knuefermann P., Hoeft A., et al. Toll-like receptor 4 deficiency: smaller infarcts, but no gain in function. BMC Physiol. 7 (2007) 5
14. Ghanem A., Troatz C., Elhafi N., Dewald O., Heeschen C., Nickenig N., et al. Quantitation of myocardial borderzone using reconstructive three-dimensional echocardiography after chronic infarction in rats - incremental value of low-dose dobutamine. Ultrasound Med. Biol. 34 (2008) 559-566
15. Agrawal S., Anderson P., Durbeej M., van R.N., Ivars F., Opdenakker G., et al. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 203 (2006) 1007-1019
16. Oh L.Y., Larsen P.H., Krekoski C.A., Edwards D.R., Donovan F., Werb Z., et al. Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J. Neurosci. 19 (1999) 8464-8475
17. Miller D.L., Driscoll E.M., Dou C., Armstrong W.F., and Lucchesi B.R. Microvascular permeabilization and cardiomyocyte injury provoked by myocardial contrast echocardiography in a canine model. J. Am. Coll. Cardiol. 47 (2006) 1464-1468
18. Miller D.L., Li P., Dou C., Armstrong W.F., and Gordon D. Evans blue staining of cardiomyocytes induced by myocardial contrast echocardiography in rats: evidence for necrosis instead of apoptosis. Ultrasound Med. Biol. 33 (2007) 1988-1996
19. Miller D.L., and Gies R.A. The influence of ultrasound frequency and gas-body composition on the contrast agent-mediated enhancement of vascular bioeffects in mouse intestine. Ultrasound Med. Biol. 26 (2000) 307-313
20. de Jong N., Emmer M., Chin C.T., Bouakaz A., Mastik F., Lohse D., et al. "Compression-only" behavior of phospholipid-coated contrast bubbles. Ultrasound Med. Biol. 33 (2007) 653-656
21. Segers V.F., Van R.I., Andries L.J., Lemmens K., Demolder M.J., De Becker A.J., et al. Mesenchymal stem cell adhesion to cardiac microvascular endothelium: activators and mechanisms. Am. J. Physiol, Heart Circ. Physiol. 290 (2006) H1370-H1377
22. Reil J.C., Gilles S., Zahler S., Brandl A., Drexler H., Hultner L., et al. Insights from knock-out models concerning postischemic release of TNFalpha from isolated mouse hearts. J. Mol. Cell. Cardiol. 42 (2007) 133-141
23. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284 (1999) 143-147
24. Templin C., Kotlarz D., Marquart F., Faulhaber J., Brendecke V., Schaefer A., et al. Transcoronary delivery of bone marrow cells to the infarcted murine myocardium: feasibility, cellular kinetics, and improvement in cardiac function. Basic Res. Cardiol. 101 (2006) 301-310
25. Miller D.L., Li P., Dou C., Gordon D., Edwards C.A., and Armstrong W.F. Influence of contrast agent dose and ultrasound exposure on cardiomyocyte injury induced by myocardial contrast echocardiography in rats. Radiology 237 (2005) 137-143
26. J. Alter, C.A. Sennoga, D.M. Lopes, R.J. Eckersley, D.J. Wells, Microbubble stability is a major determinant of the efficiency of ultrasound and microbubble mediated in vivo gene transfer. Ultrasound Med Biol 2009;35(6):976-84.