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Published in: Cardiovascular Ultrasound 1/2013

Open Access 01-04-2013 | Review

Gene therapy for cardiovascular disease mediated by ultrasound and microbubbles

Authors: Zhi-Yi Chen, Yan Lin, Feng Yang, Lan Jiang, Shu ping Ge

Published in: Cardiovascular Ultrasound | Issue 1/2013

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Abstract

Gene therapy provides an efficient approach for treatment of cardiovascular disease. To realize the therapeutic effect, both efficient delivery to the target cells and sustained expression of transgenes are required. Ultrasound targeted microbubble destruction (UTMD) technique has become a potential strategy for target-specific gene and drug delivery. When gene-loaded microbubble is injected, the ultrasound-mediated microbubble destruction may spew the transported gene to the targeted cells or organ. Meanwhile, high amplitude oscillations of microbubbles increase the permeability of capillary and cell membrane, facilitating uptake of the released gene into tissue and cell. Therefore, efficiency of gene therapy can be significantly improved. To date, UTMD has been successfully investigated in many diseases, and it has achieved outstanding progress in the last two decades. Herein, we discuss the current status of gene therapy of cardiovascular diseases, and reviewed the progress of the delivery of genes to cardiovascular system by UTMD.
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Literature
1.
go back to reference Gaziano TA: Economic burden and the cost-effectiveness of treatment of cardiovascular diseases in Africa. Heart. 2008, 94: 140-144. 10.1136/hrt.2007.128785CrossRefPubMed Gaziano TA: Economic burden and the cost-effectiveness of treatment of cardiovascular diseases in Africa. Heart. 2008, 94: 140-144. 10.1136/hrt.2007.128785CrossRefPubMed
2.
go back to reference Fishbein I, Chorny M, Levy RJ: Site-specific gene therapy for cardiovascular disease. Curr Opin Drug Discov Devel. 2010, 13: 203-213.PubMedPubMedCentral Fishbein I, Chorny M, Levy RJ: Site-specific gene therapy for cardiovascular disease. Curr Opin Drug Discov Devel. 2010, 13: 203-213.PubMedPubMedCentral
3.
go back to reference Won YW, Lee M, Kim HA, Bull DA, Kim SW: Hypoxia-inducible plasmid expressing both miSHP-1 and HO-1 for the treatment of ischemic disease. J Control Release. 2013, 165: 22-28. 10.1016/j.jconrel.2012.10.014CrossRefPubMed Won YW, Lee M, Kim HA, Bull DA, Kim SW: Hypoxia-inducible plasmid expressing both miSHP-1 and HO-1 for the treatment of ischemic disease. J Control Release. 2013, 165: 22-28. 10.1016/j.jconrel.2012.10.014CrossRefPubMed
4.
go back to reference Guo X, Huang L: Recent advances in nonviral vectors for gene delivery. Acc Chem Res. 2012, 45: 971-979. 10.1021/ar200151mCrossRefPubMed Guo X, Huang L: Recent advances in nonviral vectors for gene delivery. Acc Chem Res. 2012, 45: 971-979. 10.1021/ar200151mCrossRefPubMed
5.
go back to reference Chen ZY, Liang K, Qiu RX, Luo LP: Ultrasound- and liposome microbubble-mediated targeted gene transfer to cardiomyocytes in vivo accompanied by polyethylenimine. J Ultrasound Med. 2011, 30: 1247-1258.PubMed Chen ZY, Liang K, Qiu RX, Luo LP: Ultrasound- and liposome microbubble-mediated targeted gene transfer to cardiomyocytes in vivo accompanied by polyethylenimine. J Ultrasound Med. 2011, 30: 1247-1258.PubMed
6.
go back to reference Chen Z, Xie M, Wang X, Lv Q, Ding S: Efficient gene delivery to myocardium with ultrasound targeted microbubble destruction and polyethylenimine. J Huazhong Univ Sci Technolog Med Sci. 2008, 28 (5): 613-617. 10.1007/s11596-008-0528-4CrossRefPubMed Chen Z, Xie M, Wang X, Lv Q, Ding S: Efficient gene delivery to myocardium with ultrasound targeted microbubble destruction and polyethylenimine. J Huazhong Univ Sci Technolog Med Sci. 2008, 28 (5): 613-617. 10.1007/s11596-008-0528-4CrossRefPubMed
7.
go back to reference Chen ZY, Liang K, Sheng XJ, Si-Tu B, Sun XF, Liu JQ, Qiu RX, Zhang H, Li YW, Zhou XX, Yu JX: Optimization and apoptosis induction by RNAi with UTMD technology in vitro. Oncol Lett. 2012, 3: 1030-1036.PubMedPubMedCentral Chen ZY, Liang K, Sheng XJ, Si-Tu B, Sun XF, Liu JQ, Qiu RX, Zhang H, Li YW, Zhou XX, Yu JX: Optimization and apoptosis induction by RNAi with UTMD technology in vitro. Oncol Lett. 2012, 3: 1030-1036.PubMedPubMedCentral
8.
go back to reference Logeart D, Hatem SN, Heimburger M, Le Roux A, Michel JB, Mercadier JJ: How to optimize in vivo gene transfer to cardiac myocytes: mechanical or pharmacological procedures?. Hum Gene Ther. 2001, 12 (Seppl 1): 1601-1610.CrossRefPubMed Logeart D, Hatem SN, Heimburger M, Le Roux A, Michel JB, Mercadier JJ: How to optimize in vivo gene transfer to cardiac myocytes: mechanical or pharmacological procedures?. Hum Gene Ther. 2001, 12 (Seppl 1): 1601-1610.CrossRefPubMed
9.
go back to reference Chen ZY, Liang K, Xie MX, Wang XF, Lü Q, Zhang J: Induced apoptosis with ultrasound-mediated microbubble destruction and shRNA targeting survivin in transplanted tumors. Adv Ther. 2008, 26: 99-106.CrossRefPubMed Chen ZY, Liang K, Xie MX, Wang XF, Lü Q, Zhang J: Induced apoptosis with ultrasound-mediated microbubble destruction and shRNA targeting survivin in transplanted tumors. Adv Ther. 2008, 26: 99-106.CrossRefPubMed
10.
go back to reference Nabel EG, Plautz G, Boyce FM, Stanley JC, Nabel GJ: Recombinant gene expression in vivo within endothelial cells of the arterial wall. Science. 1989, 244: 1342-1344. 10.1126/science.2499928CrossRefPubMed Nabel EG, Plautz G, Boyce FM, Stanley JC, Nabel GJ: Recombinant gene expression in vivo within endothelial cells of the arterial wall. Science. 1989, 244: 1342-1344. 10.1126/science.2499928CrossRefPubMed
11.
go back to reference Su CH, Wu YJ, Wang HH, Yeh HI: Nonviral gene therapy targeting cardiovascular system. Am J Physiol Heart Circ Physiol. 2012, 303: H629-H638. 10.1152/ajpheart.00126.2012CrossRefPubMed Su CH, Wu YJ, Wang HH, Yeh HI: Nonviral gene therapy targeting cardiovascular system. Am J Physiol Heart Circ Physiol. 2012, 303: H629-H638. 10.1152/ajpheart.00126.2012CrossRefPubMed
12.
go back to reference Raake PW, Hinkel R, Müller S, Delker S, Kreuzpointner R, Kupatt C, Katus HA, Kleinschmidt JA, Boekstegers P, Müller OJ: Cardio-specific long-term gene expression in a porcine model after selective pressure-regulated retroinfusion of adeno-associated viral (AAV) vectors. Gene Ther. 2008, 15: 12-17. 10.1038/sj.gt.3303035CrossRefPubMed Raake PW, Hinkel R, Müller S, Delker S, Kreuzpointner R, Kupatt C, Katus HA, Kleinschmidt JA, Boekstegers P, Müller OJ: Cardio-specific long-term gene expression in a porcine model after selective pressure-regulated retroinfusion of adeno-associated viral (AAV) vectors. Gene Ther. 2008, 15: 12-17. 10.1038/sj.gt.3303035CrossRefPubMed
13.
go back to reference Peng CA: Analysis of gene transfer rate with immobilized retroviral vectors. Ann N Y Acad Sci. 2009, 1161: 26-33. 10.1111/j.1749-6632.2009.04096.xCrossRefPubMed Peng CA: Analysis of gene transfer rate with immobilized retroviral vectors. Ann N Y Acad Sci. 2009, 1161: 26-33. 10.1111/j.1749-6632.2009.04096.xCrossRefPubMed
14.
go back to reference Beronja S, Livshits G, Williams S, Fuchs E: Rapid functional dissection of genetic networks via tissue-specific transduction and RNAi in mouse embryos. Nat Med. 2010, 16: 821-827. 10.1038/nm.2167CrossRefPubMedPubMedCentral Beronja S, Livshits G, Williams S, Fuchs E: Rapid functional dissection of genetic networks via tissue-specific transduction and RNAi in mouse embryos. Nat Med. 2010, 16: 821-827. 10.1038/nm.2167CrossRefPubMedPubMedCentral
15.
go back to reference Yao XL, Yoshioka Y, Ruan GX, Chen YZ, Mizuguchi H, Mukai Y, Okada N, Gao JQ, Nakagawa S: Optimization and internalization mechanisms of PEGylated adenovirus vector with targeting peptide for cancer gene therapy. Biomacromolecules. 2012, 13: 2402-2409. 10.1021/bm300665uCrossRefPubMed Yao XL, Yoshioka Y, Ruan GX, Chen YZ, Mizuguchi H, Mukai Y, Okada N, Gao JQ, Nakagawa S: Optimization and internalization mechanisms of PEGylated adenovirus vector with targeting peptide for cancer gene therapy. Biomacromolecules. 2012, 13: 2402-2409. 10.1021/bm300665uCrossRefPubMed
16.
go back to reference Prunier F, Kawase Y, Gianni D, Scapin C, Danik SB, Ellinor PT, Hajjar RJ, Del Monte F: Prevention of ventricular arrhythmias with sarcoplasmic reticulum Ca2+ ATPase pump overexpression in a porcine model of ischemia reperfusion. Circulation. 2008, 118: 614-624. 10.1161/CIRCULATIONAHA.108.770883CrossRefPubMed Prunier F, Kawase Y, Gianni D, Scapin C, Danik SB, Ellinor PT, Hajjar RJ, Del Monte F: Prevention of ventricular arrhythmias with sarcoplasmic reticulum Ca2+ ATPase pump overexpression in a porcine model of ischemia reperfusion. Circulation. 2008, 118: 614-624. 10.1161/CIRCULATIONAHA.108.770883CrossRefPubMed
17.
go back to reference Suckau L, Fechner H, Chemaly E, Krohn S, Hadri L, Kockskämper J, Westermann D, Bisping E, Ly H, Wang X, Kawase Y, Chen J, Liang L, Sipo I, Vetter R, Weger S, Kurreck J, Erdmann V, Tschope C, Pieske B, Lebeche D, Schultheiss HP, Hajjar RJ, Poller WC: Long-term cardiac-targeted RNA interference for the treatment of heart failure restores cardiac function and reduces pathological hypertrophy. Circulation. 2009, 119: 1241-1252. 10.1161/CIRCULATIONAHA.108.783852CrossRefPubMedPubMedCentral Suckau L, Fechner H, Chemaly E, Krohn S, Hadri L, Kockskämper J, Westermann D, Bisping E, Ly H, Wang X, Kawase Y, Chen J, Liang L, Sipo I, Vetter R, Weger S, Kurreck J, Erdmann V, Tschope C, Pieske B, Lebeche D, Schultheiss HP, Hajjar RJ, Poller WC: Long-term cardiac-targeted RNA interference for the treatment of heart failure restores cardiac function and reduces pathological hypertrophy. Circulation. 2009, 119: 1241-1252. 10.1161/CIRCULATIONAHA.108.783852CrossRefPubMedPubMedCentral
18.
go back to reference Cavazzana-Calvo M, Fischer A: Gene therapy for severe combined immunodeficiency: are we there yet?. J Clin Invest. 2007, 117: 1456-1465. 10.1172/JCI30953CrossRefPubMedPubMedCentral Cavazzana-Calvo M, Fischer A: Gene therapy for severe combined immunodeficiency: are we there yet?. J Clin Invest. 2007, 117: 1456-1465. 10.1172/JCI30953CrossRefPubMedPubMedCentral
19.
go back to reference Wang Z, Storb R, Lee D, Kushmerick MJ, Chu B, Berger C, Arnett A, Allen J, Chamberlain JS, Riddell SR, Tapscott SJ: Immune responses to AAV in canine muscle monitored by cellular assays and noninvasive imaging. Mol Ther. 2010, 18: 617-624. 10.1038/mt.2009.294CrossRefPubMed Wang Z, Storb R, Lee D, Kushmerick MJ, Chu B, Berger C, Arnett A, Allen J, Chamberlain JS, Riddell SR, Tapscott SJ: Immune responses to AAV in canine muscle monitored by cellular assays and noninvasive imaging. Mol Ther. 2010, 18: 617-624. 10.1038/mt.2009.294CrossRefPubMed
20.
go back to reference Wilson JM: Lessons learned from the gene therapy trial for ornithine transcarbamylase deficiency. Mol Genet Metab. 2009, 96: 151-157. 10.1016/j.ymgme.2008.12.016CrossRefPubMed Wilson JM: Lessons learned from the gene therapy trial for ornithine transcarbamylase deficiency. Mol Genet Metab. 2009, 96: 151-157. 10.1016/j.ymgme.2008.12.016CrossRefPubMed
21.
go back to reference Zheng XZ, Hong LL, Du LF, Wang HP, Qing Gu Q: In vivo and in vitro effects of ultrasound or/and microbubbles on recombinant adeno-associated virus-mediated transgene expression in the retina. Asian Biomed. 2009, 3: 497-506. Zheng XZ, Hong LL, Du LF, Wang HP, Qing Gu Q: In vivo and in vitro effects of ultrasound or/and microbubbles on recombinant adeno-associated virus-mediated transgene expression in the retina. Asian Biomed. 2009, 3: 497-506.
22.
go back to reference Wu J, Zhang S, Wu X, Dong X, Xu P, Liu X, Li C, Huang Q: Enhanced transduction and improved photoreceptor survival of retinal degeneration by the combinatorial use of rAAV2 with a lower dose of adenovirus. Vision Res. 2008, 48: 1648-1654. 10.1016/j.visres.2008.04.019CrossRefPubMed Wu J, Zhang S, Wu X, Dong X, Xu P, Liu X, Li C, Huang Q: Enhanced transduction and improved photoreceptor survival of retinal degeneration by the combinatorial use of rAAV2 with a lower dose of adenovirus. Vision Res. 2008, 48: 1648-1654. 10.1016/j.visres.2008.04.019CrossRefPubMed
23.
go back to reference Park HJ, Yang F, Cho SW: Nonviral delivery of genetic medicine for therapeutic angiogenesis. Adv Drug Deliv Rev. 2012, 64: 40-52. 10.1016/j.addr.2011.09.005CrossRefPubMed Park HJ, Yang F, Cho SW: Nonviral delivery of genetic medicine for therapeutic angiogenesis. Adv Drug Deliv Rev. 2012, 64: 40-52. 10.1016/j.addr.2011.09.005CrossRefPubMed
24.
25.
go back to reference Ko YT, Hartner WC, Kale A, Torchilin VP: Gene delivery into ischemic myocardium by double-targeted lipoplexes with anti-myosin antibody and TAT peptide. Gene Ther. 2009, 16: 52-59. 10.1038/gt.2008.135CrossRefPubMed Ko YT, Hartner WC, Kale A, Torchilin VP: Gene delivery into ischemic myocardium by double-targeted lipoplexes with anti-myosin antibody and TAT peptide. Gene Ther. 2009, 16: 52-59. 10.1038/gt.2008.135CrossRefPubMed
26.
go back to reference Charoensit P, Kawakami S, Higuchi Y, Yamashita F, Hashida M: Enhanced growth inhibition of metastatic lung tumors by intravenous injection of ATRA-cationic liposome/IL-12 pDNA complexes in mice. Cancer Gene Ther. 2010, 17: 512-522. 10.1038/cgt.2010.12CrossRefPubMed Charoensit P, Kawakami S, Higuchi Y, Yamashita F, Hashida M: Enhanced growth inhibition of metastatic lung tumors by intravenous injection of ATRA-cationic liposome/IL-12 pDNA complexes in mice. Cancer Gene Ther. 2010, 17: 512-522. 10.1038/cgt.2010.12CrossRefPubMed
27.
go back to reference Durieux AC, Bonnefoy R, Busso T, Freyssenet D: In vivo gene electrotransfer into skeletal muscle: effects of plasmid DNA on the occurrence and extent of muscle damage. J Gene Med. 2004, 6: 809-816. 10.1002/jgm.534CrossRefPubMed Durieux AC, Bonnefoy R, Busso T, Freyssenet D: In vivo gene electrotransfer into skeletal muscle: effects of plasmid DNA on the occurrence and extent of muscle damage. J Gene Med. 2004, 6: 809-816. 10.1002/jgm.534CrossRefPubMed
29.
go back to reference Arvanitis CD, Bazan-Peregrino M, Rifai B, Seymour LW, Coussios CC: Cavitation-enhanced extravasation for drug delivery. Ultrasound Med Biol. 2011, 37: 1838-1852. 10.1016/j.ultrasmedbio.2011.08.004CrossRefPubMed Arvanitis CD, Bazan-Peregrino M, Rifai B, Seymour LW, Coussios CC: Cavitation-enhanced extravasation for drug delivery. Ultrasound Med Biol. 2011, 37: 1838-1852. 10.1016/j.ultrasmedbio.2011.08.004CrossRefPubMed
30.
go back to reference Li P, Zheng Y, Ran H, Tan J, Lin Y, Zhang Q, Ren J, Wang Z: Ultrasound-mediated targeted microbubbles: a new vehicle for cancer therapy. Frontiers Chem Sci Eng. 2013, 7: 20-28. 10.1007/s11705-013-1311-z.CrossRef Li P, Zheng Y, Ran H, Tan J, Lin Y, Zhang Q, Ren J, Wang Z: Ultrasound-mediated targeted microbubbles: a new vehicle for cancer therapy. Frontiers Chem Sci Eng. 2013, 7: 20-28. 10.1007/s11705-013-1311-z.CrossRef
31.
go back to reference Daigeler A, Chromik AM, Haendschke K, Emmelmann S, Siepmann M, Hensel K, Schmitz G, Klein-Hitpass L, Steinau HU, Lehnhardt M, Hauser J: Synergistic effects of sonoporation and taurolidin/TRAIL on apoptosis in human fibrosarcoma. Ultrasound Med Biol. 2010, 36: 1893-1906. 10.1016/j.ultrasmedbio.2010.08.009CrossRefPubMed Daigeler A, Chromik AM, Haendschke K, Emmelmann S, Siepmann M, Hensel K, Schmitz G, Klein-Hitpass L, Steinau HU, Lehnhardt M, Hauser J: Synergistic effects of sonoporation and taurolidin/TRAIL on apoptosis in human fibrosarcoma. Ultrasound Med Biol. 2010, 36: 1893-1906. 10.1016/j.ultrasmedbio.2010.08.009CrossRefPubMed
32.
go back to reference Luo J, Zhou X, Diao L, Wang Z: Experimental research on wild-type p53 plasmid transfected into retinoblastoma cells and tissues using an ultrasound microbubble intensifier. J Int Med Res. 2010, 38: 1005-1015.CrossRefPubMed Luo J, Zhou X, Diao L, Wang Z: Experimental research on wild-type p53 plasmid transfected into retinoblastoma cells and tissues using an ultrasound microbubble intensifier. J Int Med Res. 2010, 38: 1005-1015.CrossRefPubMed
33.
go back to reference Suzuki J, Ogawa M, Takayama K, Taniyama Y, Morishita R, Hirata Y, Nagai R, Isobe M: Ultrasound-microbubble-mediated intercellular adhesion molecule-1 small interfering ribonucleic acid transfection attenuates neointimal formation after arterial injury in mice. J Am Coll Cardiol. 2010, 55: 904-913. 10.1016/j.jacc.2009.09.054CrossRefPubMed Suzuki J, Ogawa M, Takayama K, Taniyama Y, Morishita R, Hirata Y, Nagai R, Isobe M: Ultrasound-microbubble-mediated intercellular adhesion molecule-1 small interfering ribonucleic acid transfection attenuates neointimal formation after arterial injury in mice. J Am Coll Cardiol. 2010, 55: 904-913. 10.1016/j.jacc.2009.09.054CrossRefPubMed
34.
go back to reference Zhou S, Li S, Liu Z, Tang Y, Wang Z, Gong J, Liu C: Ultrasound-targeted microbubble destruction mediated herpes simplex virus-thymidine kinase gene treats hepatoma in mice. J Exp Clin Cancer Res. 2010, 29: 170- 10.1186/1756-9966-29-170CrossRefPubMedPubMedCentral Zhou S, Li S, Liu Z, Tang Y, Wang Z, Gong J, Liu C: Ultrasound-targeted microbubble destruction mediated herpes simplex virus-thymidine kinase gene treats hepatoma in mice. J Exp Clin Cancer Res. 2010, 29: 170- 10.1186/1756-9966-29-170CrossRefPubMedPubMedCentral
35.
go back to reference Nayak S, Herzog RW: Progress and prospects: immune responses to viral vectors. Gene Ther. 2010, 17: 295-304. 10.1038/gt.2009.148CrossRefPubMed Nayak S, Herzog RW: Progress and prospects: immune responses to viral vectors. Gene Ther. 2010, 17: 295-304. 10.1038/gt.2009.148CrossRefPubMed
36.
go back to reference Chen Z, Liang K, Liu J, Xie M, Wang X, Lü Q, Zhang J, Fang L: Enhancement of survivin gene downregulation and cell apoptosis by a novel combination: liposome microbubbles and ultrasound exposure. Medical Oncology. 2009, 26: 491-500. 10.1007/s12032-008-9161-0CrossRefPubMed Chen Z, Liang K, Liu J, Xie M, Wang X, Lü Q, Zhang J, Fang L: Enhancement of survivin gene downregulation and cell apoptosis by a novel combination: liposome microbubbles and ultrasound exposure. Medical Oncology. 2009, 26: 491-500. 10.1007/s12032-008-9161-0CrossRefPubMed
37.
go back to reference Qiu L, Zhang L, Wang L, Jiang Y, Luo Y, Peng Y, Lin L: Ultrasound-targeted microbubble destruction enhances naked plasmid DNA transfection in rabbit Achilles tendons in vivo. Gene Ther. 2012, 19: 703-710. 10.1038/gt.2011.165CrossRefPubMed Qiu L, Zhang L, Wang L, Jiang Y, Luo Y, Peng Y, Lin L: Ultrasound-targeted microbubble destruction enhances naked plasmid DNA transfection in rabbit Achilles tendons in vivo. Gene Ther. 2012, 19: 703-710. 10.1038/gt.2011.165CrossRefPubMed
38.
go back to reference Phillips LC, Klibanov AL, Wamhoff BR, Hossack JA: Targeted gene transfection from microbubbles into vascular smooth muscle cells using focused, ultrasound-mediated delivery. Ultrasound Med Biol. 2010, 36: 1470-1480. 10.1016/j.ultrasmedbio.2010.06.010CrossRefPubMedPubMedCentral Phillips LC, Klibanov AL, Wamhoff BR, Hossack JA: Targeted gene transfection from microbubbles into vascular smooth muscle cells using focused, ultrasound-mediated delivery. Ultrasound Med Biol. 2010, 36: 1470-1480. 10.1016/j.ultrasmedbio.2010.06.010CrossRefPubMedPubMedCentral
39.
go back to reference Wang Y, Zhou J, Zhang Y, Wang X, Chen J: Delivery of TFPI-2 using SonoVue and adenovirus results in the suppression of thrombosis and arterial re-stenosis. Exp Biol Med. 2010, 235: 1072-1081. 10.1258/ebm.2010.010046.CrossRef Wang Y, Zhou J, Zhang Y, Wang X, Chen J: Delivery of TFPI-2 using SonoVue and adenovirus results in the suppression of thrombosis and arterial re-stenosis. Exp Biol Med. 2010, 235: 1072-1081. 10.1258/ebm.2010.010046.CrossRef
40.
go back to reference Tinkov S, Coester C, Serba S, Geis NA, Katus HA, Winter G, Bekeredjian R: New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: in-vivo characterization. J Control Release. 2010, 148: 368-372. 10.1016/j.jconrel.2010.09.004CrossRefPubMed Tinkov S, Coester C, Serba S, Geis NA, Katus HA, Winter G, Bekeredjian R: New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: in-vivo characterization. J Control Release. 2010, 148: 368-372. 10.1016/j.jconrel.2010.09.004CrossRefPubMed
41.
go back to reference Fujii H, Sun Z, Li SH, Wu J, Fazel S, Weisel RD, Rakowski H, Lindner J, Li RK: Ultrasound-targeted gene delivery induces angiogenesis after a myocardial infarction in mice. JACC Cardiovasc Imaging. 2009, 2: 869-879. 10.1016/j.jcmg.2009.04.008CrossRefPubMed Fujii H, Sun Z, Li SH, Wu J, Fazel S, Weisel RD, Rakowski H, Lindner J, Li RK: Ultrasound-targeted gene delivery induces angiogenesis after a myocardial infarction in mice. JACC Cardiovasc Imaging. 2009, 2: 869-879. 10.1016/j.jcmg.2009.04.008CrossRefPubMed
42.
go back to reference Stride E: Physical principles of microbubbles for ultrasound imaging and therapy. Cerebrovasc Dis. 2009, 27 (Suppl 2): 1-13.CrossRefPubMed Stride E: Physical principles of microbubbles for ultrasound imaging and therapy. Cerebrovasc Dis. 2009, 27 (Suppl 2): 1-13.CrossRefPubMed
43.
go back to reference Lentacker I, Wang N, Vandenbroucke RE, Demeester J, De Smedt SC, Sanders NN: Ultrasound exposure of lipoplex loaded microbubbles facilitates direct cytoplasmic entry of the lipoplexes. Mol Pharm. 2009, 6: 457-467. 10.1021/mp800154sCrossRefPubMed Lentacker I, Wang N, Vandenbroucke RE, Demeester J, De Smedt SC, Sanders NN: Ultrasound exposure of lipoplex loaded microbubbles facilitates direct cytoplasmic entry of the lipoplexes. Mol Pharm. 2009, 6: 457-467. 10.1021/mp800154sCrossRefPubMed
44.
go back to reference Li W, Kong F, Li X, Dai X, Liu X, Zheng Q, Wu R, Zhou X, Lü F, Chang B, Li Q, Hauswirth WW, Qu J, Pang JJ: Gene therapy following subretinal AAV5 vector delivery is not affected by a previous intravitreal AAV5 vector administration in the partner eye. Mol Vis. 2009, 15: 267-275.PubMedPubMedCentral Li W, Kong F, Li X, Dai X, Liu X, Zheng Q, Wu R, Zhou X, Lü F, Chang B, Li Q, Hauswirth WW, Qu J, Pang JJ: Gene therapy following subretinal AAV5 vector delivery is not affected by a previous intravitreal AAV5 vector administration in the partner eye. Mol Vis. 2009, 15: 267-275.PubMedPubMedCentral
45.
go back to reference Stieger K, Schroeder J, Provost N, Mendes-Madeira A, Belbellaa B, Le Meur G, Weber M, Deschamps JY, Lorenz B, Moullier P, Rolling F: Detection of intact rAAV particles up to 6 years after successful gene transfer in the retina of dogs and primates. Mol Ther. 2009, 17: 516-523. 10.1038/mt.2008.283CrossRefPubMed Stieger K, Schroeder J, Provost N, Mendes-Madeira A, Belbellaa B, Le Meur G, Weber M, Deschamps JY, Lorenz B, Moullier P, Rolling F: Detection of intact rAAV particles up to 6 years after successful gene transfer in the retina of dogs and primates. Mol Ther. 2009, 17: 516-523. 10.1038/mt.2008.283CrossRefPubMed
46.
go back to reference Chen S, Shohet RV, Bekeredjian R, Frenkel P, Grayburn PA: Optimization of ultrasound parameters for cardiac gene delivery of adenoviral or plasmid deoxyribonucleic acid by ultrasound-targeted microbubble destruction. J Am Coll Cardiol. 2003, 42: 301-308. 10.1016/S0735-1097(03)00627-2CrossRefPubMed Chen S, Shohet RV, Bekeredjian R, Frenkel P, Grayburn PA: Optimization of ultrasound parameters for cardiac gene delivery of adenoviral or plasmid deoxyribonucleic acid by ultrasound-targeted microbubble destruction. J Am Coll Cardiol. 2003, 42: 301-308. 10.1016/S0735-1097(03)00627-2CrossRefPubMed
47.
go back to reference Chen S, Shimoda M, Chen J, Grayburn PA: Stimulation of adult resident cardiac progenitor cells by durable myocardial expression of thymosin beta 4 with ultrasound-targeted microbubble delivery. Gene Ther. 2012, 20: 225-233.CrossRefPubMed Chen S, Shimoda M, Chen J, Grayburn PA: Stimulation of adult resident cardiac progenitor cells by durable myocardial expression of thymosin beta 4 with ultrasound-targeted microbubble delivery. Gene Ther. 2012, 20: 225-233.CrossRefPubMed
48.
go back to reference Hernot S, Klibanov AL: Microbubbles in ultrasound-triggered drug and gene delivery. Adv Drug Deliv Rev. 2008, 60: 1153-1166. 10.1016/j.addr.2008.03.005CrossRefPubMedPubMedCentral Hernot S, Klibanov AL: Microbubbles in ultrasound-triggered drug and gene delivery. Adv Drug Deliv Rev. 2008, 60: 1153-1166. 10.1016/j.addr.2008.03.005CrossRefPubMedPubMedCentral
49.
go back to reference Müller OJ, Schinkel S, Kleinschmidt JA, Katus HA, Bekeredjian R: Augmentation of AAV-mediated cardiac gene transfer after systemic administration in adult rats. Gene Ther. 2008, 15: 1558-1565. 10.1038/gt.2008.111CrossRefPubMed Müller OJ, Schinkel S, Kleinschmidt JA, Katus HA, Bekeredjian R: Augmentation of AAV-mediated cardiac gene transfer after systemic administration in adult rats. Gene Ther. 2008, 15: 1558-1565. 10.1038/gt.2008.111CrossRefPubMed
50.
go back to reference Beeri R: New efficient catheter-based system for myocardial gene delivery. Circulation. 2002, 106: 1756-1759. 10.1161/01.CIR.0000035240.92015.E4CrossRefPubMed Beeri R: New efficient catheter-based system for myocardial gene delivery. Circulation. 2002, 106: 1756-1759. 10.1161/01.CIR.0000035240.92015.E4CrossRefPubMed
51.
go back to reference Howard CM, Forsberg F, Minimo C, Liu JB, Merton DA, Claudio PP: Ultrasound guided site specific gene delivery system using adenoviral vectors and commercial ultrasound contrast agents. J Cell Physiol. 2006, 209: 413-421. 10.1002/jcp.20736CrossRefPubMed Howard CM, Forsberg F, Minimo C, Liu JB, Merton DA, Claudio PP: Ultrasound guided site specific gene delivery system using adenoviral vectors and commercial ultrasound contrast agents. J Cell Physiol. 2006, 209: 413-421. 10.1002/jcp.20736CrossRefPubMed
52.
go back to reference Naka T, Sakoda T, Doi T, Tsujino T, Masuyama T, Kawashima S, Iwasaki T, Ohyanagi M: Ultrasound enhances retrovirus‐mediated gene transfer. Prep Biochem Biotechnol. 2007, 37: 87-99. 10.1080/10826060701199007CrossRefPubMed Naka T, Sakoda T, Doi T, Tsujino T, Masuyama T, Kawashima S, Iwasaki T, Ohyanagi M: Ultrasound enhances retrovirus‐mediated gene transfer. Prep Biochem Biotechnol. 2007, 37: 87-99. 10.1080/10826060701199007CrossRefPubMed
53.
go back to reference Lee YH, Peng CA: Enhanced retroviral gene delivery in ultrasonic standing wave fields. Gene Ther. 2005, 12: 625-633. 10.1038/sj.gt.3302444CrossRefPubMed Lee YH, Peng CA: Enhanced retroviral gene delivery in ultrasonic standing wave fields. Gene Ther. 2005, 12: 625-633. 10.1038/sj.gt.3302444CrossRefPubMed
54.
go back to reference Taylor SL, Rahim AA, Bush NL, Bamber JC, Porter CD: Targeted retroviral gene delivery using ultrasound. J Gene Med. 2007, 9: 77-87. 10.1002/jgm.1003CrossRefPubMed Taylor SL, Rahim AA, Bush NL, Bamber JC, Porter CD: Targeted retroviral gene delivery using ultrasound. J Gene Med. 2007, 9: 77-87. 10.1002/jgm.1003CrossRefPubMed
55.
go back to reference Geers B, Lentacker I, Alonso A, Sanders NN, Demeester J, Meairs S, De Smedt SC: Elucidating the mechanisms behind sonoporation with adeno-associated virus-loaded microbubbles. Mol Pharm. 2011, 8: 2244-2251. 10.1021/mp200112yCrossRefPubMed Geers B, Lentacker I, Alonso A, Sanders NN, Demeester J, Meairs S, De Smedt SC: Elucidating the mechanisms behind sonoporation with adeno-associated virus-loaded microbubbles. Mol Pharm. 2011, 8: 2244-2251. 10.1021/mp200112yCrossRefPubMed
56.
go back to reference Xu YL, Gao YH, Liu Z, Tan KB, Hua X, Fang ZQ, Wang YL, Wang YJ, Xia HM, Zhuo ZX: 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. 10.1016/j.ijcard.2009.03.071CrossRefPubMed Xu YL, Gao YH, Liu Z, Tan KB, Hua X, Fang ZQ, Wang YL, Wang YJ, Xia HM, Zhuo ZX: 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. 10.1016/j.ijcard.2009.03.071CrossRefPubMed
57.
go back to reference Huang SL, Kee PH, Kim H, Moody MR, Chrzanowski SM, Macdonald RC, McPherson DD: Nitric oxide-loaded echogenic liposomes for nitric oxide delivery and inhibition of intimal hyperplasia. J Am Coll Cardiol. 2009, 54: 652-659. 10.1016/j.jacc.2009.04.039CrossRefPubMedPubMedCentral Huang SL, Kee PH, Kim H, Moody MR, Chrzanowski SM, Macdonald RC, McPherson DD: Nitric oxide-loaded echogenic liposomes for nitric oxide delivery and inhibition of intimal hyperplasia. J Am Coll Cardiol. 2009, 54: 652-659. 10.1016/j.jacc.2009.04.039CrossRefPubMedPubMedCentral
58.
go back to reference Saliba Y, Mougenot N, Jacquet A, Atassi F, Hatem S, Farès N, Lompré AM: A new method of ultrasonic nonviral gene delivery to the adult myocardium. J Mol Cell Cardiol. 2012, 53: 801-808. 10.1016/j.yjmcc.2012.07.016CrossRefPubMed Saliba Y, Mougenot N, Jacquet A, Atassi F, Hatem S, Farès N, Lompré AM: A new method of ultrasonic nonviral gene delivery to the adult myocardium. J Mol Cell Cardiol. 2012, 53: 801-808. 10.1016/j.yjmcc.2012.07.016CrossRefPubMed
59.
go back to reference Zhao YZ, Lu CT, Li XK, Tang QQ, Tian XQ, Zhao YP, Zhang Y, Tian JL, Yang W, Ge S, Nair CK, Shen X: Improving the cardio protective effect of aFGF in ischemic myocardium with ultrasound-mediated cavitation of heparin modified microbubbles: preliminary experiment. J Drug Target. 2012, 20: 623-631. 10.3109/1061186X.2012.702771CrossRefPubMed Zhao YZ, Lu CT, Li XK, Tang QQ, Tian XQ, Zhao YP, Zhang Y, Tian JL, Yang W, Ge S, Nair CK, Shen X: Improving the cardio protective effect of aFGF in ischemic myocardium with ultrasound-mediated cavitation of heparin modified microbubbles: preliminary experiment. J Drug Target. 2012, 20: 623-631. 10.3109/1061186X.2012.702771CrossRefPubMed
60.
go back to reference Sun L, Huang CW, Wu J, Chen KJ, Li SH, Weisel RD, Rakowski H, Sung HW, Li RK: The use of cationic microbubbles to improve ultrasound-targeted gene delivery to the ischemic myocardium. Biomaterials. 2013, 34: 2107-2116. 10.1016/j.biomaterials.2012.11.041CrossRefPubMed Sun L, Huang CW, Wu J, Chen KJ, Li SH, Weisel RD, Rakowski H, Sung HW, Li RK: The use of cationic microbubbles to improve ultrasound-targeted gene delivery to the ischemic myocardium. Biomaterials. 2013, 34: 2107-2116. 10.1016/j.biomaterials.2012.11.041CrossRefPubMed
61.
go back to reference Phillips LC, Klibanov AL, Wamhoff BR, Hossack JA: Intravascular ultrasound detection and delivery of molecularly targeted microbubbles for gene delivery. IEEE Trans Ultrason Ferroelectr Freq Control. 2012, 59: 1596-1601.CrossRefPubMed Phillips LC, Klibanov AL, Wamhoff BR, Hossack JA: Intravascular ultrasound detection and delivery of molecularly targeted microbubbles for gene delivery. IEEE Trans Ultrason Ferroelectr Freq Control. 2012, 59: 1596-1601.CrossRefPubMed
62.
go back to reference Ferrara K, Pollard R, Borden M: Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu Rev Biomed Eng. 2007, 9: 415-447. 10.1146/annurev.bioeng.8.061505.095852CrossRefPubMed Ferrara K, Pollard R, Borden M: Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu Rev Biomed Eng. 2007, 9: 415-447. 10.1146/annurev.bioeng.8.061505.095852CrossRefPubMed
63.
go back to reference Ji S, Jun J, Xiaohan Y: Study on construction of Nano tPA plasmid to prevent thrombosis after mechanical valve replacement in dogs. J Surg Res. 2011, 168: e1-e5. 10.1016/j.jss.2010.01.011CrossRefPubMed Ji S, Jun J, Xiaohan Y: Study on construction of Nano tPA plasmid to prevent thrombosis after mechanical valve replacement in dogs. J Surg Res. 2011, 168: e1-e5. 10.1016/j.jss.2010.01.011CrossRefPubMed
64.
go back to reference Ren ST, Zhang H, Wang YW, Jing BB, Li YX, Liao YR, Kang XN, Zang WJ, Wang B: The preparation of a new self-made microbubble-loading urokinase and its thrombolysis combined with low-frequency ultrasound in vitro. Ultrasound Med Biol. 2011, 37: 1828-1837. 10.1016/j.ultrasmedbio.2011.06.018CrossRefPubMed Ren ST, Zhang H, Wang YW, Jing BB, Li YX, Liao YR, Kang XN, Zang WJ, Wang B: The preparation of a new self-made microbubble-loading urokinase and its thrombolysis combined with low-frequency ultrasound in vitro. Ultrasound Med Biol. 2011, 37: 1828-1837. 10.1016/j.ultrasmedbio.2011.06.018CrossRefPubMed
65.
go back to reference Mannell H, Pircher J, Räthel T, Schilberg K, Zimmermann K, Pfeifer A, Mykhaylyk O, Gleich B, Pohl U, Krötz F: Targeted endothelial gene delivery by ultrasonic destruction of magnetic microbubbles carrying lentiviral vectors. Pharm Res. 2012, 29: 1282-1294. 10.1007/s11095-012-0678-8CrossRefPubMed Mannell H, Pircher J, Räthel T, Schilberg K, Zimmermann K, Pfeifer A, Mykhaylyk O, Gleich B, Pohl U, Krötz F: Targeted endothelial gene delivery by ultrasonic destruction of magnetic microbubbles carrying lentiviral vectors. Pharm Res. 2012, 29: 1282-1294. 10.1007/s11095-012-0678-8CrossRefPubMed
66.
go back to reference Takeshita F, Ochiya T: Therapeutic potential of RNA interference against cancer. Cancer Sci. 2006, 97: 689-696. 10.1111/j.1349-7006.2006.00234.xCrossRefPubMed Takeshita F, Ochiya T: Therapeutic potential of RNA interference against cancer. Cancer Sci. 2006, 97: 689-696. 10.1111/j.1349-7006.2006.00234.xCrossRefPubMed
67.
go back to reference Kupatt C: Nonviral intercellular adhesion molecule-1 small interfering ribonucleic acid sequences transfection in vivo how ultrasound bursts into therapy. J Am Coll Cardiol. 2010, 55: 914-916. 10.1016/j.jacc.2009.10.036CrossRefPubMed Kupatt C: Nonviral intercellular adhesion molecule-1 small interfering ribonucleic acid sequences transfection in vivo how ultrasound bursts into therapy. J Am Coll Cardiol. 2010, 55: 914-916. 10.1016/j.jacc.2009.10.036CrossRefPubMed
68.
go back to reference Kinoshita M, Hynynen K: A novel method for the intracellular delivery of siRNA using microbubble-enhanced focused ultrasound. Biochem Biophys Res Commun. 2005, 335: 393-399. 10.1016/j.bbrc.2005.07.101CrossRefPubMed Kinoshita M, Hynynen K: A novel method for the intracellular delivery of siRNA using microbubble-enhanced focused ultrasound. Biochem Biophys Res Commun. 2005, 335: 393-399. 10.1016/j.bbrc.2005.07.101CrossRefPubMed
69.
go back to reference Ghanem A, Steingen C, Brenig F, Funcke F, Bai ZY, Hall C, Chin CT, Nickenig 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. 10.1016/j.yjmcc.2009.06.008CrossRefPubMed Ghanem A, Steingen C, Brenig F, Funcke F, Bai ZY, Hall C, Chin CT, Nickenig 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. 10.1016/j.yjmcc.2009.06.008CrossRefPubMed
70.
go back to reference Otani K, Yamahara K, Ohnishi S, Obata H, Kitamura S, Nagaya N: Nonviral delivery of siRNA into mesenchymal stem cells by a combination of ultrasound and microbubbles. J Control Release. 2009, 133: 146-153. 10.1016/j.jconrel.2008.09.088CrossRefPubMed Otani K, Yamahara K, Ohnishi S, Obata H, Kitamura S, Nagaya N: Nonviral delivery of siRNA into mesenchymal stem cells by a combination of ultrasound and microbubbles. J Control Release. 2009, 133: 146-153. 10.1016/j.jconrel.2008.09.088CrossRefPubMed
71.
go back to reference Toma C, Fisher A, Wang J, Chen X, Grata M, Leeman J, Winston B, Kaya M, Fu H, Lavery L, Fischer D, Wagner WR, Villanueva FS: Vascular endoluminal delivery of mesenchymal stem cells using acoustic radiation force. Tissue Eng Part A. 2011, 17: 1457-1464. 10.1089/ten.tea.2010.0539CrossRefPubMedPubMedCentral Toma C, Fisher A, Wang J, Chen X, Grata M, Leeman J, Winston B, Kaya M, Fu H, Lavery L, Fischer D, Wagner WR, Villanueva FS: Vascular endoluminal delivery of mesenchymal stem cells using acoustic radiation force. Tissue Eng Part A. 2011, 17: 1457-1464. 10.1089/ten.tea.2010.0539CrossRefPubMedPubMedCentral
Metadata
Title
Gene therapy for cardiovascular disease mediated by ultrasound and microbubbles
Authors
Zhi-Yi Chen
Yan Lin
Feng Yang
Lan Jiang
Shu ping Ge
Publication date
01-04-2013
Publisher
BioMed Central
Published in
Cardiovascular Ultrasound / Issue 1/2013
Electronic ISSN: 1476-7120
DOI
https://doi.org/10.1186/1476-7120-11-11

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