Targeted renal therapies through microbubbles and ultrasound

Advanced Drug Delivery Reviews

Volumn 62, Issue 14, 2010, Pages 1369-1377

  Deelman, Leo E ^a   Declèves, Anne Emilie ^b   Rychak, Joshua J ^c   Sharma, Kumar ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c Targeson Inc   (United States)

Author keywords

Bioeffects; Contrast agents; Drug delivery; Kidney; Microbubbles; Molecular imaging; Targeted microbubbles; Ultrasound

Indexed keywords

BIO-EFFECTS; CONTRAST AGENT; KIDNEY; MICROBUBBLES; MOLECULAR IMAGING; TARGETED MICROBUBBLES; ULTRASOUND;

DRUG DELIVERY;

ULTRASONICS;

INTERCELLULAR ADHESION MOLECULE 1; MUCOSAL ADDRESSIN CELLULAR ADHESION MOLECULE 1 ANTIBODY; PADGEM PROTEIN; SELECTIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA ANTIBODY; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

CELL TRANSPORT; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG HALF LIFE; DRUG RELEASE; GENE TARGETING; GENETIC TRANSFECTION; GLOMERULUS FILTRATION; HUMAN; KIDNEY; KIDNEY DISEASE; KIDNEY ISCHEMIA; MICROBUBBLE; NONHUMAN; PLASMID; PRIORITY JOURNAL; RENOGRAPHY; REPERFUSION INJURY; REVIEW;

ANIMALS; CONTRAST MEDIA; DRUG DELIVERY SYSTEMS; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; INJECTIONS, INTRAVENOUS; KIDNEY; KIDNEY DISEASES; MICROBUBBLES; RABBITS; RATS; SWINE; ULTRASONICS;

EID: 78649447847     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.addr.2010.10.002     Document Type: Review

References (112)

1. Kaul S. Myocardial contrast echocardiography: a 25-year retrospective. Circulation 2008, 118:291-308.
2. Swinburn J.M., Lahiri A., Senior R. Intravenous myocardial contrast echocardiography predicts recovery of dysynergic myocardium early after acute myocardial infarction. J. Am. Coll. Cardiol. 2001, 38:19-25.
3. Sieswerda G.T., Yang L., Boo M.B., Kamp O. Real-time perfusion imaging: a new echocardiographic technique for simultaneous evaluation of myocardial perfusion and contraction. Echocardiography 2003, 20:545-555.
4. Tachibana K., Uchida T., Ogawa K., Yamashita N., Tamura K. Induction of cell-membrane porosity by ultrasound. Lancet 1999, 353:1409.
5. Meijering B.D., Juffermans L.J., Van W.A., Henning R.H., Zuhorn I.S., Emmer M., Versteilen A.M., Paulus W.J., Van Gilst W.H., Kooiman K., de Jong N., Musters R.J., Deelman L.E., Kamp O. Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation. Circ. Res. 2009, 104:679-687.
6. 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.
7. 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.
8. Korpanty G., Chen S., Shohet R.V., Ding J., Yang B., Frenkel P.A., Grayburn P.A. Targeting of VEGF-mediated angiogenesis to rat myocardium using ultrasonic destruction of microbubbles. Gene Ther. 2005, 12:1305-1312.
9. 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.
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. Porter T.R., Hiser W.L., Kricsfeld D., Deligonul U., Xie F., Iversen P., Radio S. Inhibition of carotid artery neointimal formation with intravenous microbubbles. Ultrasound Med. Biol. 2001, 27:259-265.
12. Taniyama Y., Tachibana K., Hiraoka K., Namba T., Yamasaki K., Hashiya N., Aoki M., Ogihara T., Yasufumi K., Morishita R. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 2002, 105:1233-1239.
13. Hashiya N., Aoki M., Tachibana K., Taniyama Y., Yamasaki K., Hiraoka K., Makino H., Yasufumi K., Ogihara T., Morishita R. Local delivery of E2F decoy oligodeoxynucleotides using ultrasound with microbubble agent (Optison) inhibits intimal hyperplasia after balloon injury in rat carotid artery model. Biochem. Biophys. Res. Commun. 2004, 317:508-514.
14. Teupe C., Richter S., Fisslthaler B., Randriamboavonjy V., Ihling C., Fleming I., Busse R., Zeiher A.M., Dimmeler S. Vascular gene transfer of phosphomimetic endothelial nitric oxide synthase (S1177D) using ultrasound-enhanced destruction of plasmid-loaded microbubbles improves vasoreactivity. Circulation 2002, 105:1104-1109.
15. 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.
16. Skyba D.M., Price R.J., Linka A.Z., Skalak T.C., Kaul S. Direct in vivo visualization of intravascular destruction of microbubbles by ultrasound and its local effects on tissue. Circulation 1998, 98:290-293.
17. Deelman L., Sharma K. Mechanisms of kidney fibrosis and the role of antifibrotic therapies. Curr. Opin. Nephrol. Hypertens. 2009, 18:85-90.
18. Sharma K., McGowan T.A. TGF-beta in diabetic kidney disease: role of novel signaling pathways. Cytokine Growth Factor Rev. 2000, 11:115-123.
19. Sharma K., Jin Y., Guo J., Ziyadeh F.N. Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes 1996, 45:522-530.
20. Ziyadeh F.N., Hoffman B.B., Han D.C., Iglesias-De La Cruz M.C., Hong S.W., Isono M., Chen S., McGowan T.A., Sharma K. Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc. Natl Acad. Sci. USA 2000, 97:8015-8020.
21. Chen S., Iglesias-De La Cruz M.C., Jim B., Hong S.W., Isono M., Ziyadeh F.N. Reversibility of established diabetic glomerulopathy by anti-TGF-beta antibodies in db/db mice. Biochem. Biophys. Res. Commun. 2003, 300:16-22.
22. Juarez P., Vilchis-Landeros M.M., Ponce-Coria J., Mendoza V., Hernandez-Pando R., Bobadilla N.A., Lopez-Casillas F. Soluble betaglycan reduces renal damage progression in db/db mice. Am. J. Physiol. Ren. Physiol. 2007, 292:F321-F329.
23. Schneider M. Characteristics of SonoVuetrade mark. Echocardiography 1999, 16:743-746.
24. Walday P., Tolleshaug H., Gjoen T., Kindberg G.M., Berg T., Skotland T., Holtz E. Biodistributions of air-filled albumin microspheres in rats and pigs. Biochem. J. 1994, 299(Pt 2):437-443.
25. Perkins A.C., Frier M., Hindle A.J., Blackshaw P.E., Bailey S.E., Hebden J.M., Middleton S.M., Wastie M.L. Human biodistribution of an ultrasound contrast agent (Quantison) by radiolabelling and gamma scintigraphy. Br. J. Radiol. 1997, 70:603-611.
26. Tartis M.S., Kruse D.E., Zheng H., Zhang H., Kheirolomoom A., Marik J., Ferrara K.W. Dynamic microPET imaging of ultrasound contrast agents and lipid delivery. J. Control. Release 2008, 131:160-166.
27. Walday P., Tolleshaug H., Gjoen T., Kindberg G.M., Berg T., Skotland T., Holtz E. Biodistributions of air-filled albumin microspheres in rats and pigs. Biochem. J. 1994, 299(Pt 2):437-443.
28. Wei K., Le E., Bin J.P., Coggins M., Thorpe J., Kaul S. Quantification of renal blood flow with contrast-enhanced ultrasound. J. Am. Coll. Cardiol. 2001, 37:1135-1140.
29. Kalantarinia K., Belcik J.T., Patrie J.T., Wei K. Real-time measurement of renal blood flow in healthy subjects using contrast-enhanced ultrasound. Am. J. Physiol. Ren. Physiol. 2009, 297:F1129-F1134.
30. Correas J.M., Claudon M., Tranquart F., Helenon A.O. The kidney: imaging with microbubble contrast agents. Ultrasound Q. 2006, 22:53-66.
31. Sullivan J.C., Wang B., Boesen E.I., D'Angelo G., Pollock J.S., Pollock D.M. Novel use of ultrasound to examine regional blood flow in the mouse kidney. Am. J. Physiol. Ren. Physiol. 2009, 297:F228-F235.
32. Lindner J.R., Song J., Xu F., Klibanov A.L., Singbartl K., Ley K., Kaul S. Noninvasive ultrasound imaging of inflammation using microbubbles targeted to activated leukocytes. Circulation 2000, 102:2745-2750.
33. Bayfield M.S., Lindner J.R., Kaul S., Ismail S., Sheil M.L., Goodman N.C., Zacour R., Spotnitz W.D. Deoxygenated blood minimizes adherence of sonicated albumin microbubbles during cardioplegic arrest and after blood reperfusion: experimental and clinical observations with myocardial contrast echocardiography. J. Thorac. Cardiovasc. Surg. 1997, 113:1100-1108.
34. Lindner J.R., Coggins M.P., Kaul S., Klibanov A.L., Brandenburger G.H., Ley K. Microbubble persistence in the microcirculation during ischemia/reperfusion and inflammation is caused by integrin- and complement-mediated adherence to activated leukocytes. Circulation 2000, 101:668-675.
35. Takeuchi H., Ohmori K., Kondo I., Shinomiya K., Oshita A., Takagi Y., Yoshida J., Mizushige K., Kohno M. Interaction with leukocytes: phospholipid-stabilized versus albumin-shell microbubbles. Radiology 2004, 230:735-742.
36. Dayton P.A., Chomas J.E., Lum A.F., Allen J.S., Lindner J.R., Simon S.I., Ferrara K.W. Optical and acoustical dynamics of microbubble contrast agents inside neutrophils. Biophys. J. 2001, 80:1547-1556.
37. Korosoglou G., Hardt S.E., Bekeredjian R., Jenne J., Konstantin M., Hagenmueller M., Katus H.A., Kuecherer H. Ultrasound exposure can increase the membrane permeability of human neutrophil granulocytes containing microbubbles without causing complete cell destruction. Ultrasound Med. Biol. 2006, 32:297-303.
38. Aggeli C., Giannopoulos G., Lampropoulos K., Pitsavos C., Stefanadis C. Adverse bioeffects of ultrasound contrast agents used in echocardiography: true safety issue or "much ado about nothing"?. Curr. Vasc. Pharmacol. 2009, 7:338-346.
39. Wu J., Nyborg W.L. Ultrasound, cavitation bubbles and their interaction with cells. Adv. Drug Deliv. Rev. 2008, 60:1103-1116.
40. Miller D.L., Averkiou M.A., Brayman A.A., Everbach E.C., Holland C.K., Wible J.H., Wu J. Bioeffects considerations for diagnostic ultrasound contrast agents. J. Ultrasound Med. 2008, 27:611-632.
41. 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.
42. Miller D.L., Dou C., Wiggins R.C., Wharram B.L., Goyal M., Williams A.R. An in vivo rat model simulating imaging of human kidney by diagnostic ultrasound with gas-body contrast agent. Ultrasound Med. Biol. 2007, 33:129-135.
43. Jimenez C., de Gracia R., Aguilera A., Alonso S., Cirugeda A., Benito J., Regojo R.M., Aguilar R., Warlters A., Gomez 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.
44. Fischer K., McDannold N.J., Zhang Y., Kardos M., Szabo A., Szabo A., Reusz G.S., Jolesz F.A. Renal ultrafiltration changes induced by focused US. Radiology 2009, 253:697-705.
45. Sica D.A. Can focused US with a diagnostic US contrast agent favorably affect renal function?. Radiology 2009, 253:577-578.
46. Porter T.R., Iversen P.L., Li S., Xie F. Interaction of diagnostic ultrasound with synthetic oligonucleotide-labeled perfluorocarbon-exposed sonicated dextrose albumin microbubbles. J. Ultrasound Med. 1996, 15:577-584.
47. Price R.J., Skyba D.M., Kaul S., Skalak T.C. Delivery of colloidal particles and red blood cells to tissue through microvessel ruptures created by targeted microbubble destruction with ultrasound. Circulation 1998, 98:1264-1267.
48. Unger E.C., McCreery T., Sweitzer R., Vielhauer G., Wu G., Shen D., Yellowhair D. MRX 501: a novel ultrasound contrast agent with therapeutic properties. Acad. Radiol. 1998, 5(Suppl 1):S247-S249.
49. Ka S.M., Huang X.R., Lan H.Y., Tsai P.Y., Yang S.M., Shui H.A., Chen A. Smad7 gene therapy ameliorates an autoimmune crescentic glomerulonephritis in mice. J. Am. Soc. Nephrol. 2007, 18:1777-1788.
50. Lan H.Y., Mu W., Tomita N., Huang X.R., Li J.H., Zhu H.J., Morishita R., Johnson R.J. Inhibition of renal fibrosis by gene transfer of inducible Smad7 using ultrasound-microbubble system in rat UUO model. J. Am. Soc. Nephrol. 2003, 14:1535-1548.
51. 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.
52. 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.
53. Ng Y.Y., Hou C.C., Wang W., Huang X.R., Lan H.Y. Blockade of NFkappaB activation and renal inflammation by ultrasound-mediated gene transfer of Smad7 in rat remnant kidney. Kidney Int. Suppl. 2005, S83-S91.
54. Negishi Y., Endo Y., Fukuyama T., Suzuki R., Takizawa T., Omata D., Maruyama K., Aramaki Y. Delivery of siRNA into the cytoplasm by liposomal bubbles and ultrasound. J. Control. Release 2008, 132:124-130.
55. Taniyama Y., Tachibana K., Hiraoka K., Namba T., Yamasaki K., Hashiya N., Aoki M., Ogihara T., Yasufumi K., Morishita R. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 2002, 105:1233-1239.
56. Akowuah E.F., Gray C., Lawrie A., Sheridan P.J., Su C.H., Bettinger T., Brisken A.F., Gunn J., Crossman D.C., Francis S.E., Baker A.H., Newman C.M. Ultrasound-mediated delivery of TIMP-3 plasmid DNA into saphenous vein leads to increased lumen size in a porcine interposition graft model. Gene Ther. 2005, 12:1154-1157.
57. Taniyama Y., Tachibana K., Hiraoka K., Aoki M., Yamamoto S., Matsumoto K., Nakamura T., Ogihara T., Kaneda Y., Morishita R. Development of safe and efficient novel nonviral gene transfer using ultrasound: enhancement of transfection efficiency of naked plasmid DNA in skeletal muscle. Gene Ther. 2002, 9:372-380.
58. 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.
59. Korpanty G., Chen S., Shohet R.V., Ding J., Yang B., Frenkel P.A., Grayburn P.A. Targeting of VEGF-mediated angiogenesis to rat myocardium using ultrasonic destruction of microbubbles. Gene Ther. 2005, 12:1305-1312.
60. Xenariou S., Griesenbach U., Liang H.D., Zhu J., Farley R., Somerton L., Singh C., Jeffery P.K., Ferrari S., Scheule R.K., Cheng S.H., Geddes D.M., Blomley M., Alton E.W. Use of ultrasound to enhance nonviral lung gene transfer in vivo. Gene Ther. 2007, 14:768-774.
61. Shen Z.P., Brayman A.A., Chen L., Miao C.H. Ultrasound with microbubbles enhances gene expression of plasmid DNA in the liver via intraportal delivery. Gene Ther. 2008, 15:1147-1155.
62. Iwanaga K., Tominaga K., Yamamoto K., Habu M., Maeda H., Akifusa S., Tsujisawa T., Okinaga T., Fukuda J., Nishihara T. Local delivery system of cytotoxic agents to tumors by focused sonoporation. Cancer Gene Ther. 2007, 14:354-363.
63. Nie F., Xu H.X., Lu M.D., Wang Y., Tang Q. Anti-angiogenic gene therapy for hepatocellular carcinoma mediated by microbubble-enhanced ultrasound exposure: an in vivo experimental study. J. Drug Target. 2008, 16:389-395.
64. Breitz H.B., Weiden P.L., Beaumier P.L., Axworthy D.B., Seiler C., Su F.M., Graves S., Bryan K., Reno J.M. Clinical optimization of pretargeted radioimmunotherapy with antibody-streptavidin conjugate and 90Y-DOTA-biotin. J. Nucl. Med. 2000, 41:131-140.
65. Pochon S., Tardy I., Bussat P., Bettinger T., Brochot J., von Wronski M., Passantino L., Schneider M. BR55: a lipopeptide-based VEGFR2-targeted ultrasound contrast agent for molecular imaging of angiogenesis. Invest. Radiol. 2010, 45:89-95.
66. Weller G.E., Wong M.K., Modzelewski R.A., Lu E., Klibanov A.L., Wagner W.R., Villanueva F.S. Ultrasonic imaging of tumor angiogenesis using contrast microbubbles targeted via the tumor-binding peptide arginine-arginine-leucine. Cancer Res. 2005, 65:533-539.
67. Pillai R., Marinelli E.R., Fan H., Nanjappan P., Song B., von Wronski M.A., Cherkaoui S., Tardy I., Pochon S., Schneider M., Nunn A.D., Swenson R.E. A phospholipid-PEG2000 conjugate of a vascular endothelial growth factor receptor 2 (VEGFR2)-targeting heterodimer peptide for contrast-enhanced ultrasound imaging of angiogenesis. Bioconjug. Chem. 2010, 21:556-562.
68. Pysz M.A., Foygel K., Rosenberg J., Gambhir S.S., Schneider M., Willmann J.K. Antiangiogenic cancer therapy: monitoring with molecular US and a clinically translatable contrast agent (BR55). Radiology 2010, 256:519-527.
69. Kindberg G.M., Tolleshaug H., Roos N., Skotland T. Hepatic clearance of sonazoid perfluorobutane microbubbles by Kupffer cells does not reduce the ability of liver to phagocytose or degrade albumin microspheres. Cell Tissue Res. 2003, 312:49-54.
70. Yanagisawa K., Moriyasu F., Miyahara T., Yuki M., Iijima H. Phagocytosis of ultrasound contrast agent microbubbles by Kupffer cells. Ultrasound Med. Biol. 2007, 33:318-325.
71. Nakano H., Ishida Y., Hatakeyama T., Sakuraba K., Hayashi M., Sakurai O., Hataya K. Contrast-enhanced intraoperative ultrasonography equipped with late Kupffer-phase image obtained by sonazoid in patients with colorectal liver metastases. World J. Gastroenterol. 2008, 14:3207-3211.
72. Hatanaka K., Kudo M., Minami Y., Ueda T., Tatsumi C., Kitai S., Takahashi S., Inoue T., Hagiwara S., Chung H., Ueshima K., Maekawa K. Differential diagnosis of hepatic tumors: value of contrast-enhanced harmonic sonography using the newly developed contrast agent. Sonazoid, Intervirology 2008, 51(Suppl 1):61-69.
73. Furusawa Y., Zhao Q.L., Hassan M.A., Tabuchi Y., Takasaki I., Wada S., Kondo T. Ultrasound-induced apoptosis in the presence of Sonazoid and associated alterations in gene expression levels: a possible therapeutic application. Cancer Lett. 2010, 288:107-115.
74. Lindner J.R., Song J., Christiansen J., Klibanov A.L., Xu F., Ley K. Ultrasound assessment of inflammation and renal tissue injury with microbubbles targeted to P-selectin. Circulation 2001, 104:2107-2112.
75. Andonian S., Coulthard T., Smith A.D., Singhal P.S., Lee B.R. Real-time quantitation of renal ischemia using targeted microbubbles: in-vivo measurement of P-selectin expression. J. Endourol. 2009, 23:373-378.
76. Takalkar A.M., Klibanov A.L., Rychak J.J., Lindner J.R., Ley K. Binding and detachment dynamics of microbubbles targeted to P-selectin under controlled shear flow. J. Control. Release 2004, 96:473-482.
77. Ferrante E.A., Pickard J.E., Rychak J., Klibanov A., Ley K. Dual targeting improves microbubble contrast agent adhesion to VCAM-1 and P-selectin under flow. J. Control. Release 2009, 140:100-107.
78. Rychak J.J., Klibanov A.L., Ley K.F., Hossack J.A. Enhanced targeting of ultrasound contrast agents using acoustic radiation force. Ultrasound Med. Biol. 2007, 33:1132-1139.
79. Tlaxca J., Anderson C., Klibanov A., Hossack J.A., Ley K. Targeted Transfection by Sonoporation in Inflammatory Bowel Disease. The Fourteenth European Symposium on Ultrasound Contrast Imaging 2009.
80. Ley K. The role of selectins in inflammation and disease. Trends Mol. Med. 2003, 9:263-268.
81. Kaufmann B.A., Carr C.L., Belcik J.T., Xie A., Yue Q., Chadderdon S., Caplan E.S., Khangura J., Bullens S., Bunting S., Lindner J.R. Molecular imaging of the initial inflammatory response in atherosclerosis: implications for early detection of disease. Arterioscler. Thromb. Vasc. Biol. 2010, 30:54-59.
82. Kaufmann B.A., Sanders J.M., Davis C., Xie A., Aldred P., Sarembock I.J., Lindner J.R. Molecular imaging of inflammation in atherosclerosis with targeted ultrasound detection of vascular cell adhesion molecule-1. Circulation 2007, 116:276-284.
83. Springer T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994, 76:301-314.
84. Villanueva F.S., Jankowski R.J., Klibanov S., Pina M.L., Alber S.M., Watkins S.C., Brandenburger G.H., Wagner W.R. Microbubbles targeted to intercellular adhesion molecule-1 bind to activated coronary artery endothelial cells. Circulation 1998, 98:1-5.
85. Weller G.E., Villanueva F.S., Klibanov A.L., Wagner W.R. Modulating targeted adhesion of an ultrasound contrast agent to dysfunctional endothelium. Ann. Biomed. Eng. 2002, 30:1012-1019.
86. Weller G.E., Lu E., Csikari M.M., Klibanov A.L., Fischer D., Wagner W.R., Villanueva F.S. Ultrasound imaging of acute cardiac transplant rejection with microbubbles targeted to intercellular adhesion molecule-1. Circulation 2003, 108:218-224.
87. Linker R.A., Reinhardt M., Bendszus M., Ladewig G., Briel A., Schirner M., Maurer M., Hauff P. In vivo molecular imaging of adhesion molecules in experimental autoimmune encephalomyelitis (EAE). J. Autoimmun. 2005, 25:199-205.
88. Reinhardt M., Hauff P., Linker R.A., Briel A., Gold R., Rieckmann P., Becker G., Toyka K.V., Maurer M., Schirner M. Ultrasound derived imaging and quantification of cell adhesion molecules in experimental autoimmune encephalomyelitis (EAE) by Sensitive Particle Acoustic Quantification (SPAQ). Neuroimage 2005, 27:267-278.
89. Bachmann C., Klibanov A.L., Olson T.S., Sonnenschein J.R., Rivera-Nieves J., Cominelli F., Ley K.F., Lindner J.R., Pizarro T.T. Targeting mucosal addressin cellular adhesion molecule (MAdCAM)-1 to noninvasively image experimental Crohn's disease. Gastroenterology 2006, 130:8-16.
90. Takada M., Nadeau K.C., Shaw G.D., Tilney N.L. Prevention of late renal changes after initial ischemia/reperfusion injury by blocking early selectin binding. Transplantation 1997, 64:1520-1525.
91. Gasser M., Waaga A.M., Kist-Van Holthe J.E., Lenhard S.M., Laskowski I., Shaw G.D., Hancock W.W., Tilney N.L. Normalization of brain death-induced injury to rat renal allografts by recombinant soluble P-selectin glycoprotein ligand. J. Am. Soc. Nephrol. 2002, 13:1937-1945.
92. Gasser M., Waaga-Gasser A.M., Grimm M.W., Grimm M.R., Lenhard M.S., Kist-Van Holthe J.E., Laskowski I., Shaw G.D., Thiede A., Hancock W.W., Tilney N.L. Selectin blockade plus therapy with low-dose sirolimus and cyclosporin a prevent brain death-induced renal allograft dysfunction. Am. J. Transplant. 2005, 5:662-670.
93. Tipping P.G., Huang X.R., Berndt M.C., Holdsworth S.R. A role for P selectin in complement-independent neutrophil-mediated glomerular injury. Kidney Int. 1994, 46:79-88.
94. Roy-Chaudhury P., Wu B., King G., Campbell M., Macleod A.M., Haites N.E., Simpson J.G., Power D.A. Adhesion molecule interactions in human glomerulonephritis: importance of the tubulointerstitium. Kidney Int. 1996, 49:127-134.
95. Brady H.R. Complex roles for P-selectin in the pathophysiology of glomerulonephritis. Curr. Opin. Nephrol. Hypertens. 1996, 5:423-426.
96. Akgur F.M., Zibari G.B., McDonald J.C., Granger D.N., Brown M.F. Effects of dextran and pentoxifylline on hemorrhagic shock-induced P-selectin expression. J. Surg. Res. 1999, 87:232-238.
97. Akgur F.M., Zibari G.B., McDonald J.C., Granger D.N., Brown M.F. Kinetics of P-selectin expression in regional vascular beds after resuscitation of hemorrhagic shock: a clue to the mechanism of multiple system organ failure. Shock 2000, 13:140-144.
98. Iwamoto M., Mizuiri S., Arita M., Hemmi H. Nuclear factor-kappaB activation in diabetic rat kidney: evidence for involvement of P-selectin in diabetic nephropathy. Tohoku J. Exp. Med. 2005, 206:163-171.
99. Hirata K., Shikata K., Matsuda M., Akiyama K., Sugimoto H., Kushiro M., Makino H. Increased expression of selectins in kidneys of patients with diabetic nephropathy. Diabetologia 1998, 41:185-192.
100. Sharma K., Jin Y., Guo J., Ziyadeh F.N. Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes 1996, 45:522-530.
101. Lucas C., Bald L.N., Fendly B.M., Mora-Worms M., Figari I.S., Patzer E.J., Palladino M.A. The autocrine production of transforming growth factor-beta 1 during lymphocyte activation. A study with a monoclonal antibody-based ELISA. J. Immunol. 1990, 145:1415-1422.
102. Pochon S., Tardy I., Bussat P., Bettinger T., Brochot J., von Wronski M., Passantino L., Schneider M. BR55: a lipopeptide-based VEGFR2-targeted ultrasound contrast agent for molecular imaging of angiogenesis. Invest. Radiol. 2010, 45:89-95.
103. Willmann J.K., Lutz A.M., Paulmurugan R., Patel M.R., Chu P., Rosenberg J., Gambhir S.S. Dual-targeted contrast agent for US assessment of tumor angiogenesis in vivo. Radiology 2008, 248:936-944.
104. Rychak J.J., Graba J., Cheung A.M., Mystry B.S., Lindner J.R., Kerbel R.S., Foster F.S. Microultrasound molecular imaging of vascular endothelial growth factor receptor 2 in a mouse model of tumor angiogenesis. Mol. Imaging 2007, 6:289-296.
105. Willmann J.K., Paulmurugan R., Chen K., Gheysens O., Rodriguez-Porcel M., Lutz A.M., Chen I.Y., Chen X., Gambhir S.S. US imaging of tumor angiogenesis with microbubbles targeted to vascular endothelial growth factor receptor type 2 in mice. Radiology 2008, 246:508-518.
106. Dayton P.A., Pearson D., Clark J., Simon S., Schumann P.A., Zutshi R., Matsunaga T.O., Ferrara K.W. Ultrasonic analysis of peptide- and antibody-targeted microbubble contrast agents for molecular imaging of alphavbeta3-expressing cells. Mol. Imaging 2004, 3:125-134.
107. Leong-Poi H., Christiansen J., Klibanov A.L., Kaul S., Lindner J.R. Noninvasive assessment of angiogenesis by ultrasound and microbubbles targeted to alpha(v)-integrins. Circulation 2003, 107:455-460.
108. Ellegala D.B., Leong-Poi H., Carpenter J.E., Klibanov A.L., Kaul S., Shaffrey M.E., Sklenar J., Lindner J.R. Imaging tumor angiogenesis with contrast ultrasound and microbubbles targeted to alpha(v)beta3. Circulation 2003, 108:336-341.
109. De Vriese A.S., Tilton R.G., Stephan C.C., Lameire N.H. Vascular endothelial growth factor is essential for hyperglycemia-induced structural and functional alterations of the peritoneal membrane. J. Am. Soc. Nephrol. 2001, 12:1734-1741.
110. Flyvbjerg A., Gnaes-Hansen F., De Vriese A.S., Schrijvers B.F., Tilton R.G., Rasch R. Amelioration of long-term renal changes in obese type 2 diabetic mice by a neutralizing vascular endothelial growth factor antibody. Diabetes 2002, 51:3090-3094.
111. Dayton P.A., Zhao S., Bloch S.H., Schumann P., Penrose K., Matsunaga T.O., Zutshi R., Doinikov A., Ferrara K.W. Application of ultrasound to selectively localize nanodroplets for targeted imaging and therapy. Mol. Imaging 2006, 5:160-174.
112. Rapoport N., Kennedy A.M., Shea J.E., Scaife C.L., Nam K.H. Ultrasonic nanotherapy of pancreatic cancer: lessons from ultrasound imaging. Mol. Pharm. 2009, 7:22-31.