Targeted Delivery of Bone Mesenchymal Stem Cells by Ultrasound Destruction of Microbubbles Promotes Kidney Recovery in Acute Kidney Injury

Ultrasound in Medicine and Biology

Volumn 38, Issue 4, 2012, Pages 661-669

  Tang, Hai Lin ^a,b   Wang, Zhi Gang ^b   Li, Qiao ^b   Ran, Hai Tao ^b   Zheng, Yuan Yi ^b   Ren, Jian Li ^b   Ling, Zhi Yu ^b   Li, Ao ^b   Zhao, Bowen ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b THE SECOND AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Acute tubular necrosis; Homing; Mesenchymal stem cell; Microbubble; Ultrasound

Indexed keywords

ACOUSTIC EXPOSURE; ACUTE TUBULAR NECROSIS; ADHESION MOLECULES; BONE MARROW MESENCHYMAL STEM CELLS; CONTROL GROUPS; ENGRAFTMENT; EPIDERMAL GROWTH FACTORS; HEPATOCYTE GROWTH FACTOR; HISTOLOGICAL EXAMINATION; HOMING; KIDNEY TISSUES; MERCURIC CHLORIDE; MESENCHYMAL STEM CELL; MICRO-BUBBLE; MICROBUBBLES; MODEL GROUPS; RAT MODEL; REAL-TIME POLYMERASE CHAIN REACTION; TARGETED DELIVERY; ULTRASOUND DESTRUCTION; WESTERN BLOTTING; WESTERN-BLOT ANALYSIS;

ADHESION; CHLORINE COMPOUNDS; FLOWCHARTING; FLUORESCENCE MICROSCOPY; MERCURY COMPOUNDS; MOLECULAR BIOLOGY; POLYMERASE CHAIN REACTION; RATS; RECOVERY; RNA; STEM CELLS; TISSUE; ULTRASONICS;

CELL CULTURE;

4',6 DIAMIDINO 2 PHENYLINDOLE; EPIDERMAL GROWTH FACTOR; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; SCATTER FACTOR;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL HOMING; CELL LABELING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE SEVERITY; ECHOGRAPHY; FLUORESCENCE MICROSCOPY; HISTOPATHOLOGY; KIDNEY TUBULE NECROSIS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROBUBBLE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RADIATION EXPOSURE; RAT; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ACUTE KIDNEY INJURY; ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; INDOLES; INTERCELLULAR ADHESION MOLECULE-1; MICROBUBBLES; MICROSCOPY, FLUORESCENCE; PHENOTYPE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; ULTRASONICS;

EID: 84863282047     PISSN: 03015629     EISSN: 1879291X     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2012.01.003     Document Type: Article

References (30)

1. Bekeredjian R., Chen S., Frenkel P.A., Grayburn P.A., Shohet R.V. Ultrasound targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 2003, 108:1022-1026.
2. Chavakis E., Urbich C., Dimmeler S. Homing and engraftment of progenitor cells: A prerequisite for cell therapy. J Mol Cell Cardiol 2008, 45:514-522.
3. Chiusolo A., Defazio R., Casartelli A., Bocchini N., Mongillo M., Zanetti E., Cristofori P., Trevisan A. Regucalcin down-regulation in rat kidney tissue after treatment with nephrotoxicants. Toxicol Lett 2008, 182:84-90.
4. Duffield J.S., Bonventre J.V. Kidney tubular epithelium is restored without replacement with bone marrow-derived cells during repair after ischemic injury. Kidney Int 2005, 68:1956-1961.
5. Duffield J.S., Park K.M., Hsiao L.L., Kelley V.R., Scadden D.T., Ichimura T., Bonventre J.V. Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 2005, 115:1743-1755.
6. Fujiyama S., Amano K., Uehira K., Yoshida M., Nishiwaki Y., Nozawa Y., Jin D., Takai S., Miyazaki M., Egashira K., Imada T., Iwasaka T. Bone marrow monocyte lineage cells adhere on injured endothelium in a monocyte chemoattractant protein-1-dependent manner and accelerate re-endothelialization as endothelial progenitor cells. Circ Res 2003, 93:980-989.
7. Ghanem A., Steinqen C., Breniq F., Funcke F., Bai Z.Y., Hall C., Chin C.T., Nickeniq G., Bloch W., Tiemann K. Focused ultrasound-induced stimulation of microbubbles augments site-targeted engraftment of mesenchymal stem cells after acute myocardial infarction. J Mol Cell Cardiol 2009, 47:411-418.
8. Gleason M., Gosselin R., Hodge D. Clinical toxicology of commercial products 1957, Williams & Wilkins, Baltimore.
9. Herrera M.B., Bussolati B., Bruno S., Fonsato V., Romanazzi G.M., Camussi G. Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int J Mol Med 2004, 14:1035-1041.
10. Hou C.C., Wang W., Huang X.R., Fu P., Chen T.H., Sheikh-Hamad D., Lan H.Y. Ultrasound-microbubble-mediated gene transfer of inducible Smad7 blocks transforming growth factor-beta signaling and fibrosis in rat remnant kidney. Am J Pathol 2005, 166:761-771.
11. Humes H.D., Cieslinski D.A., Coimbra T.M., Messana J.M., Galvao C. Epidermal growth factor enhances renal tubular cell regeneration, and repair and accelerates the recovery of renal function in postischemic acute renal failure. J Clin Invest 1989, 84:1757-1761.
12. 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 2005, 25:2128-2134.
13. Jimenez C., de Gracia R., Aguilera A., Alonso S., Cirugeda A., Benito J., Regojo R.M., Aguilar R., Warlters A., Gómez R., Largo C., Selgas R. In situ kidney insonation with microbubble contrast agents does not cause renal tissue damage in a porcine model. J Ultrasound Med 2008, 27:1607-1615.
14. Kale S., Karihaloo A., Clark P.R., Kashgarian M., Krause D.S., Cantley L.G. Bone marrow stem cells contribute to repair of the ischemically injured renal tubule. J Clin Invest 2003, 112:42-49.
15. Kato M., McDonald K.J., Khan S., Ross I.L., Vuckovic S., Chen K., Munster D., MacDonald K.P., Hart D.N. Expression of human DEC -205(CD 205) multilectin receptor on leukocytes. Int Immunol 2006, 18:857-869.
16. 1H NMR) in rats. Toxicol Appl Pharmacol 2010, 249:114-126.
17. Koike H., Tomita N., Azuma H., Taniyama Y., Yamasaki K., Kunugiza Y., Tachibana K., Ogihara T., Morishita R. An efficient gene transfer method mediated by ultrasound and microbubbles into the kidney. J Gene Med 2005, 7:108-116.
18. Kondo I., Ohmori K., Oshita A., Takeuchi H., Fuke S., Shinomiya K., Noma T., Namba T., Kohno M. Treatment of acute myocardial infarction by hepatocyte growth factor gene transfer: The first demonstration of myocardial transfer of a "functional" gene using ultrasonic microbubble destruction. J Am Coll Cardiol 2004, 44:644-653.
19. Lin F., Moran A., Igarashi P. Intrarenal cells, not bone marrow-derived cells, are the major source for regeneration in postischemic kidney. J Clin Invest 2005, 115:1756-1764.
20. Matsumoto K., Nakamura T. Hepatocyte growth factor: Renotropic role and potential therapeutics for renal diseases. Kidney Int 2001, 59:2023-2038.
21. Morigi M., Imberti B., Zoja C., Corna D., Tomasoni S., Abbate M., Rottoli D., Angioletti S., Benigni A., Perico N., Alison M., Remuzzi G. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 2004, l15:1794-1804.
22. Ren J.L., Wang Z.G., Zhang Y., Zheng Y.Y., Li X.S., Zhang Q.X., Wang Z.X., Xu C.S. Transfection efficiency of TDL compound in HUVEC enhanced by ultrasound-targeted microbubble destruction. Ultrasound Med Biol 2008, 34:1857-1867.
23. Song J., Chappell J.C., Qi M., VanGieson E.J., Kaul S., Price R.J. Influence of injection site, microvascular pressure and ultrasound variables on microbubble-mediated delivery of microspheres to muscle. J Am Coll Cardiol 2002, 39:726-731.
24. Suzuki K., Murtuza B., Beauchamp J.R., Brand N.J., Barton P.J., Varela-Carver A., Fukushima S., Coppen S.R., Partridge T.A., Yacoub M.H. Role of interleukin-1ß in acute inflammation and graft death after cell transplantation to the heart. Circulation 2004, 110:219-224.
25. Togel F., Hu Z., Weiss K., Isaac J., Lange C., Westenfelder C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 2005, 289:31-42.
26. Togel F., Weiss K., Yang Y., Hu Z., Zhang P., Westenfelder C. Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. Am J Physiol Renal Physiol 2007, 292:1626-1635.
27. Williams A.R., Wiggins R.C., Wharram B.L., Goyal M., Dou C., Johnson K.J., Miller D.L. Nephron injury induced by diagnostic ultrasound imaging at high mechanical index with gas body contrast agent. Ultrasound Med Biol 2007, 33:1336-1344.
28. Xu Y.L., Gao Y.H., Liu Z., Tan K.B., Hua X., Fang Z.Q., Wang Y.L., Wang Y.J., Xia H.M., Zhuo Z.X. Myocardium-targeted transplantation of mesenchymal stem cells by diagnostic ultrasound-mediated microbubble destruction improves cardiac function in myocardial infarction of New Zealand rabbits. Int J Cardiol 2010, 138:182-195.
29. 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 2006, 40:799-809.
30. Zhigang W., Zhiyu L., Haitao R., Hong R., Qunxia Z., Ailong H., Qi L., Chunjing Z., Hailin T., Lin G., Mingli P., Shiyu P. Ultrasound-mediated microbubble destruction enhances VEGF gene delivery to the infarcted myocardium in rats. Clin Imaging 2004, 28:395-398.