Liposomal nanocarriers for plasminogen activators

Journal of Controlled Release

Volumn 227, Issue , 2016, Pages 45-57

  Koudelka, Stepan ^a,b   Mikulik, Robert ^b   Mašek, Josef ^a   Raška, Milan ^a,c   Turánek Knotigová, Pavlína ^a   Miller, Andrew D ^d   Turánek, Jaroslav ^a  

^a VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^b ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

^c PALACKÝ UNIVERSITY   (Czech Republic)

^d GlobalAcorn Ltd   (United Kingdom)

Author keywords

Fibrin; Liposomes; Platelets; Protein delivery; RGD peptide; Streptokinase; Stroke; Thrombus; Tissue plasminogen activator; Urokinase

Indexed keywords

DRUG THERAPY; LIPOSOMES; PLATELETS; TISSUE;

FIBRIN; PROTEIN DELIVERY; RGD PEPTIDE; STREPTOKINASE; STROKE; THROMBUS; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE;

PROTEINS;

LIPOSOME; MACROGOL; NANOCARRIER; PLASMIN; PLASMINOGEN ACTIVATOR; STAPHYLOKINASE; STREPTOKINASE; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE; AUR PROTEIN, STAPHYLOCOCCUS AUREUS; FIBRINOLYTIC AGENT; METALLOPROTEINASE; NANOMATERIAL;

DRUG TARGETING; FIBRINOLYTIC THERAPY; HUMAN; LIPOSOMAL DELIVERY; NONHUMAN; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; REVIEW; THROMBOCYTE ACTIVATION; THROMBUS; ANIMAL; CHEMISTRY; PROCEDURES; THROMBOEMBOLISM; ULTRASTRUCTURE;

ANIMALS; FIBRINOLYSIN; FIBRINOLYTIC AGENTS; HUMANS; LIPOSOMES; METALLOENDOPEPTIDASES; NANOSTRUCTURES; STREPTOKINASE; THROMBOEMBOLISM; THROMBOLYTIC THERAPY; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84959010834     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.02.019     Document Type: Review

References (109)

1. T.A. Elbayoumi, and V.P. Torchilin Liposomes for targeted delivery of antithrombotic drugs Expert Opin. Drug Deliv. 5 2008 1185 1198
2. D. Collen, and H.R. Lijnen Basic and clinical aspects of fibrinolysis and thrombolysis Blood 78 1991 3114 3124
3. A. Banerjee, Y. Chisti, and U.C. Banerjee Streptokinase: a clinically useful thrombolytic agent Biotechnol. Adv. 22 2004 287 307
4. D. Collen, and H.R. Lijnen Staphylokinase, a fibrin-specific plasminogen activator with therapeutic potential? Blood 84 1994 680 686
5. D.B. Baruah, R.N. Dash, M.R. Chaudhari, and S.S. Kadam Plasminogen activators: a comparison Vasc. Pharmacol. 44 2006 1 9
6. B. Vaidya, G.P. Agrawal, and S.P. Vyas Functionalized carriers for the improved delivery of plasminogen activators Int. J. Pharm. 424 2012 1 11
7. S. Frokjaer, and D.E. Otzen Protein drug stability: a formulation challenge Nat. Rev. Drug Discov. 4 2005 298 306
8. W. Wang Protein aggregation and its inhibition in biopharmaceutics Int. J. Pharm. 289 2005 1 30
9. W. Wei Instability, stabilization, and formulation of liquid protein pharmaceuticals Int. J. Pharm. 185 1999 129 188
10. C.F. Greineder, M.D. Howard, R. Carnemolla, D.B. Cines, and V.R. Muzykantov Advanced drug delivery systems for antithrombotic agents Blood 122 2013 1565 1575
11. H. Berger, and S.V. Pizzo Preparation of polyethylene glycol-tissue plasminogen activator adducts that retain functional activity: characteristics and behavior in three animal species Blood 71 1980 1641 1647
12. F.A. Harding, M.M. Sticker, J. Razo, and R.B. DuBridge The immunogenicity of humanized and fully human antibodies: residual immunogenicity resides in the CDR regions MAbs 2 2010 256 265
13. D.J.A. Crommelin, T. Daemen, G.L. Scherphof, M.H. Vingerhoeds, J.L.M. Heeremans, C. Kluft, and G. Storm Liposomes: vehicles for the targeted and controlled delivery of peptides and proteins J. Control. Release 46 1997 165 175
14. M.L. Tan, P.F.M. Choong, and C.R. Dass Recent developments in liposomes, microparticles and nanoparticles for protein and peptide drug delivery Peptides 31 2010 184 193
15. A. Sharma, and U.S. Sharma Liposomes in drug delivery: progress and limitations Int. J. Pharm. 154 1997 123 140
16. S.B. Kulkarni, G.V. Betageri, and M. Singh Factors affecting microencapsulation of drugs in liposomes J. Microencapsul. 12 1995 229 246
17. T.W. Chung, S.S. Wang, and W.J. Tsai Accelerating thrombolysis with chitosan-coated plasminogen activators encapsulated in poly-(lactide-co-glycolide) (PLGA) nanoparticles Biomaterials 29 2008 228 237
18. T.M. Allen, and C. Hansen Pharmacokinetics of stealth versus conventional liposomes: effect of dose Biochim. Biophys. Acta 1068 1991 133 141
19. P.S. Uster, T.M. Allen, B.E. Daniel, C.J. Mendez, M.S. Newman, and G.Z. Zhu Insertion of poly(ethylene glycol) derivatized phospholipid into preformed liposomes results in prolonged in vivo circulation time FEBS Lett. 386 1996 243 246
20. M.C. Woodle, and D.D. Lasic Sterically stabilized liposomes Biochim. Biophys. Acta 1113 1992 171 199
21. S. Zalipsky, C.B. Hansen, D.E.L. de Menezes, and T.M. Allen Long-circulating, polyethylene glycol-grafted immunoliposomes J. Control. Release 39 1996 153 161
22. D.J.A. Crommelin, G. Scherphof, and G. Storm Active targeting with particulate carrier systems in the blood compartment Adv. Drug Deliv. Rev. 17 1995 49 60
23. P. Walde, and S. Ichikawa Enzymes inside vesicles: preparation, reactivity and applications Biomol. Eng. 18 2001 143 177
24. S. Absar, K. Nahar, Y.M. Kwon, and F. Ahsan Thrombus-targeted nanocarrier attenuates bleeding complications associated with conventional thrombolytic therapy Pharm. Res. 30 2013 1663 1676
25. J.D. Castile, and K.M.G. Taylor Factors affecting the size distribution of liposomes produced by freeze-thaw extrusion Int. J. Pharm. 188 1999 87 95
26. L.M. Crowe, C. Womersley, J.H. Crowe, D. Reid, L. Appel, and A. Rudolph Prevention of fusion and leakage in freeze-dried liposomes by carbohydrates Biochim. Biophys. Acta 861 1986 131 140
27. B. Holt, and A. Sen Gupta Streptokinase loading in liposomes for vascular targeted nanomedicine applications: encapsulation efficiency and effects of processing J. Biomater. Appl. 26 2012 509 527
28. J.L.M. Heeremans, H.R. Gerritsen, S.P. Meusen, R.W. Mijnheer, R.S.G. Panday, R. Prevost, C. Kluft, and D.J.A. Crommelin The preparation of tissue-type plasminogen activator (t-PA) containing liposomes: entrapment efficiency and ultracentrifugation damage J. Drug Target. 3 1995 301 310
29. V. Ntimenou, S. Mourtas, E.V. Christodoulakis, M. Tsilimbaris, and S.G. Antimisiaris Stability of protein-encapsulating DRV liposomes after freeze-drying: a study with BSA and t-PA J. Liposome Res. 16 2006 403 416
30. P.D. Nguyen, E.A. Orear, A.E. Johnson, R. Lu, and B.M. Fung Thrombolysis using liposomal encapsulated streptokinase: an in vitro study Proc. Soc. Exp. Biol. Med. 192 1989 261 269
31. Z.L. Li, N.Z. Zhang, and Y.H. Nie Accelerated thrombolysis by liposomal-encapsulated urokinase in a canine model of acute myocardial infarction J. Chin. Med. Assoc. 74 1994 338 340
32. J.L. Rigaud, M. Chami, O. Lambert, D. Levy, and J.L. Ranck Use of detergents in two-dimensional crystallization of membrane proteins Biochim. Biophys. Acta 1508 2000 112 128
33. J.L. Rigaud, and D. Levy Reconstitution of membrane proteins into liposomes Methods Enzymol. 372 2003 65 86
34. P.L. Ahl, L. Chen, W.R. Perkins, S.R. Minchey, L.T. Boni, T.F. Taraschi, and A.S. Janoff Interdigitation-fusion: a new method for producing lipid vesicles of high internal volume Biochim. Biophys. Acta 1195 1994 237 244
35. W.R. Perkins, D.E. Vaughan, S.R. Plavin, W.L. Daley, J. Rauch, L. Lee, and A.S. Janoff Streptokinase entrapment in interdigitation-fusion liposomes improves thrombolysis in an experimental rabbit model Thromb. Haemost. 77 1997 1174 1178
36. C. Kirby, and G. Gregoriadis Dehydration-rehydration vesicles: a simple method for high yield drug entrapment in liposomes Nat. Biotechnol. 2 1984 979 984
37. F. Szoka, and D. Papahadjopoulos Procedure for preparation of liposomes with large internal aqueous space and high capture by reverse-phase evaporation Proc. Natl. Acad. Sci. U. S. A. 75 1978 4194 4198
38. R. Barnadas-Rodriguez, and M. Sabes Factors involved in the production of liposomes with a high-pressure homogenizer Int. J. Pharm. 213 2001 175 186
39. J. Turanek Fast protein liquid chromatography system as a tool for liposome preparation by the extrusion procedure Anal. Biochem. 218 1994 352 357
40. J. Masek, E. Bartheldyova, Z. Korvasova, M. Skrabalova, S. Koudelka, P. Kulich, I. Kratochvilova, A.D. Miller, M. Ledvina, M. Raska, and J. Turanek Immobilization of histidine-tagged proteins on monodisperse metallochelation liposomes: preparation and study of their structure Anal. Biochem. 408 2011 95 104
41. R.F. Schmelter, S.M. Shaw, G.S. Born, R.L. Landolt, and K.R. Hetzel A preliminary study of the association of urokinase with liposomes Can. J. Pharm. Sci. 16 1981 37 39
42. R. Carnemolla, and V.R. Muzykantov Vascular targeting of antithrombotic agents IUBMB Life 63 2011 632 639
43. H.R. Lijnen, and D. Collen Development of thrombolytic agents Biotechnol. Adv. 11 1993 115 130
44. S. Coutre, and L. Leung Novel antithrombotic therapeutics targeted against platelet glycoprotein IIb/IIIa Annu. Rev. Med. 46 1995 257 265
45. G.F. Huang, Z.M. Zhou, R. Srinivasan, M.S. Penn, K. Kottke-Marchant, R.E. Marchant, and A.S. Gupta Affinity manipulation of surface-conjugated RGD peptide to modulate binding of liposomes to activated platelets Biomaterials 29 2008 1676 1685
46. S.P. Vyas, and B. Vaidya Targeted delivery of thrombolytic agents: role of integrin receptors Expert Opin. Drug Deliv. 6 2009 499 508
47. P.D. Nguyen, E.A. Orear, A.E. Johnson, E. Patterson, T.L. Whitsett, and R. Bhakta Accelerated thrombolysis and reperfusion in a canine model of myocardial infarction by liposomal encapsulation of streptokinase Circ. Res. 66 1990 875 878
48. J.K. Leach, E.A. Orear, E. Patterson, P. Miao, and A.E. Johnson Accelerated thrombolysis in a rabbit model of carotid artery thrombosis with liposome-encapsulated and microencapsulated streptokinase Thromb. Haemost. 90 2003 64 70
49. W.L. Daley, D.E. Lapsley, and A.S. Janoff Comparative effects of streptokinase and liposome-encapsulated streptokinase on platelet aggregation in vitro J. Am. Coll. Cardiol. 31 1998 410
50. B. Khoobehi, and G.A. Peyman Accelerated thrombolysis and reperfusion in a primate model of branch vein occlusion by liposomal encapsulation of streptokinase Invest. Ophthalmol. Vis. Sci. 38 1997 4879
51. R. Smith, B. Khoobehi, and G.A. Peyman Reperfusion of branched vein occlusion using liposome-encapsulated streptokinase Invest. Ophthalmol. Vis. Sci. 36 1995 159
52. S. Erdogan, A.Y. Ozer, B. Volkan, B. Caner, and H. Bilgili Thrombus localization by using streptokinase containing vesicular systems Drug Deliv. 13 2006 303 309
53. S.H. Baek, S.J. Park, S.E. Jin, J.K. Kim, C.K. Kim, and J.M. Hwang Subconjunctivally injected, liposome-encapsulated streptokinase enhances the absorption rate of subconjunctival hemorrhages in rabbits Eur. J. Pharm. Biopharm. 72 2009 546 551
54. S.B. Han, S.H. Baek, J.S. Park, H.K. Yang, J.Y. Kim, C.K. Kim, and J.M. Hwang Effect of subconjunctivally injected liposome-encapsulated tissue plasminogen activator on the absorption rate of subconjunctival hemorrhages in rabbits Cornea 30 2011 1455 1460
55. J.W. Moon, Y.K. Song, J.P. Jee, C.K. Kim, H.K. Choung, and J.M. Hwang Effect of subconjunctivally injected, liposome-bound, low-molecular-weight heparin on the absorption rate of subconjunctival hemorrhage in rabbits Invest. Ophthalmol. Vis. Sci. 47 2006 3968 3974
56. S.E. Jin, I.S. Kim, and C.K. Kim Comparative effects of PEG-containing liposomal formulations on in vivo pharmacokinetics of streptokinase Arch. Pharm. Res. 38 2015 1822 1829
57. I.S. Kim, H.G. Choi, H.S. Choi, B.K. Kim, and C.K. Kim Prolonged systemic delivery of streptokinase using liposome Arch. Pharm. Res. 21 1998 248 252
58. A.I. Azuaga, C.M. Dobson, P.L. Mateo, and F. Conejero-Lara Unfolding and aggregation during the thermal denaturation of streptokinase Eur. J. Biochem. 269 2002 4121 4133
59. J.P. Colletier, B. Chaize, M. Winterhalter, and D. Fournier Protein encapsulation in liposomes: efficacy depends on interactions between protein and phospholipid bilayer BMC Biotechnol. 2 2002 9 16
60. A. Sen Gupta, G. Huang, B.J. Lestini, S. Sagnella, K. Kottke-Marchant, and R.E. Marchant RGD-modified liposomes targeted to activated platelets as a potential vascular drug delivery system Thromb. Haemost. 93 2005 106 114
61. V. Tsikaris The anti-platelet approach targeting the fibrinogen ligand of the GPIIb/IIIa receptor J. Pept. Sci. 10 2004 589 602
62. B.J. Lestini, S.M. Sagnella, Z. Xu, M.S. Shive, N.J. Richter, J. Jayaseharan, A.J. Case, K. Kottke-Marchant, J.M. Anderson, and R.E. Marchant Surface modification of liposomes for selective cell targeting in cardiovascular drug delivery J. Control. Release 78 2002 235 247
63. B. Vaidya, G.P. Agrawal, and S.P. Vyas Platelets directed liposomes for the delivery of streptokinase: development and characterization Eur. J. Pharm. Sci. 44 2011 589 594
64. S. Cheng, W.S. Craig, D. Mullen, J.F. Tschopp, D. Dixon, and M.D. Pierschbacher Design and synthesis of novel cyclic RGD-containing peptides as highly potent and selective integrin alpha IIb beta 3 antagonists J. Med. Chem. 37 1994 1 8
65. B. Vaidya, M.K. Nayak, D. Dash, G.P. Agrawal, and S.P. Vyas Development and characterization of site specific target sensitive liposomes for the delivery of thrombolytic agents Int. J. Pharm. 403 2011 254 261
66. S. Soeda, M. Kakiki, H. Shimeno, and A. Nagamatsu Some properties of tissue-type plasminogen activator reconstituted onto phospholipid and/or glycolipid vesicles Biochem. Biophys. Res. Commun. 146 1987 94 100
67. J.H. Crowe, L.M. Crowe, J.F. Carpenter, and C.A. Wistrom Stabilization of dry phospholipid-bilayers and proteins by sugars Biochem. J. 242 1987 1 10
68. E.C.A. van Winden Freeze-drying of liposomes: theory and practice Methods Enzymol. 367 2003 99 110
69. M.C. Woodle, K.K. Matthay, M.S. Newman, J.E. Hidayat, L.R. Collins, C. Redemann, F.J. Martin, and D. Papahadjopoulos Versatility in lipid compositions showing prolonged circulation with sterically stabilized liposomes Biochim. Biophys. Acta 1105 1992 193 200
70. J.Y. Kim, J.K. Kim, J.S. Park, Y. Byun, and C.K. Kim The use of PEGylated liposomes to prolong circulation lifetimes of tissue plasminogen activator Biomaterials 30 2009 5751 5756
71. J.L.M. Heeremans, P. Los, R. Prevost, D.J.A. Crommelin, and C. Kluft Fibrin binding of plasminogen coated liposomes in vitro Thromb. Haemost. 75 1996 134 139
72. J.L.M. Heeremans, R. Prevost, H. Feitsma, C. Kluft, and D.J.A. Crommelin Clot accumulation characteristics of plasminogen-bearing liposomes in a flow-system Thromb. Haemost. 79 1998 144 149
73. J.L.M. Heeremans, N. Los, D.J.A. Crommelin, and C. Kluft A convenient procedure for coupling the homing device glu-plasminogen to liposomes Thromb. Haemost. 65 1991 1192
74. J.L.M. Heeremans, J.J. Kraaijenga, P. Los, C. Kluft, and D.J.A. Crommelin Development of a procedure for coupling the homing device glu-plasminogen to liposomes Biochim. Biophys. Acta 1117 1992 258 264
75. J.L.M. Heeremans, F.W. Mijnheer, H.R. Gerritsen, R. Prevost, C. Kluft, and D.J.A. Crommelin Long-term stability of liposomes containing both tissue-type plasminogen activator and glu-plasminogen Int. J. Pharm. 129 1996 191 202
76. J.L.M. Heeremans, R. Prevost, M.E.A. Bekkers, P. Los, J.J. Emeis, C. Kluft, and D.J.A. Crommelin Thrombolytic treatment with tissue-type plasminogen activator (t-PA) containing liposomes in rabbits: a comparison with free t-PA Thromb. Haemost. 73 1995 488 494
77. M. Asahi, T. Rammohan, T. Sumii, X.Y. Wang, R.J. Pauw, V. Weissig, V.P. Torchilin, and E.H. Lo Antiactin-targeted immunoliposomes ameliorate tissue plasminogen activator-induced hemorrhage after focal embolic stroke J. Cereb. Blood Flow Metab. 23 2003 895 899
78. S. Ware, J.P. Donahue, J. Hawiger, and W.F. Anderson Structure of the fibrinogen gamma-chain integrin binding and factor XIIIa cross-linking sites obtained through carrier protein driven crystallization Protein Sci. 8 1999 2663 2671
79. K.Y. Ng, and Y. Liu Therapeutic ultrasound: its application in drug delivery Med. Res. Rev. 22 2002 204 223
80. S. Hernot, and A.L. Klibanov Microbubbles in ultrasound-triggered drug and gene delivery Adv. Drug Deliv. Rev. 60 2008 1153 1166
81. M. Vlasin, R. Lukac, Z. Kauerova, P. Kohout, J. Masek, E. Bartheldyova, S. Koudelka, Z. Korvasova, J. Plockova, N. Hronova, and J. Turanek Specific contrast ultrasound using sterically stabilized microbubbles for early diagnosis of thromboembolic disease in a rabbit model Can. J. Vet. Res. 78 2014 133 139
82. J.E. Chomas, P. Dayton, J. Allen, K. Morgan, and K.W. Ferrara Mechanisms of contrast agent destruction IEEE Trans. Ultrason. Ferroelectr. Freq. Control 48 2001 232 248
83. J.E. Chomas, P. Dayton, D. May, and K. Ferrara Threshold of fragmentation for ultrasonic contrast agents J. Biomed. Opt. 6 2001 141 150
84. A. Kalbanov, D. Klein, T. Pelura, E. Schutt, and J. Weers Dissolution of multicomponent microbubbles in the bloodstream: 1. Theory Ultrasound Med. Biol. 24 1998 739 749
85. J.A. Kopechek, T.M. Abruzzo, B. Wang, S.M. Chrzanowski, D.A.B. Smith, P.H. Kee, S. Huang, J.H. Collier, D.D. McPherson, and C.K. Holland Ultrasound-mediated release of hydrophilic and lipophilic agents from echogenic liposomes J. Ultrasound Med. 27 2008 1597 1606
86. J. Turanek, A.D. Miller, Z. Kauerova, R. Lukac, J. Masek, S. Koudelka, and M. Raska Lipid-based nanoparticles and microbubbles: multifunctional lipid-based biocompatible particles for in vivo imaging and theranostics P.A. Serra, Advances in Bioengineering 2015 InTech Inc. Rijeka 79 116
87. K.D. Buchanan, S. Huang, H. Kim, R.C. Macdonald, and D.D. McPherson Echogenic liposome compositions for increased retention of ultrasound reflectivity at physiologic temperature J. Pharm. Sci. 97 2008 2242 2249
88. S.D. Tiukinhoy-Laing, S.L. Huang, M. Klegerman, C.K. Holland, and D.D. McPherson Ultrasound-facilitated thrombolysis using tissue-plasminogen activator-loaded echogenic liposomes Thromb. Res. 119 2007 777 784
89. S.D. Tiukinhoy-Laing, K. Buchanan, D. Parikh, S.L. Huang, R.C. Macdonald, D.D. McPherson, and M.E. Klegerman Fibrin targeting of tissue plasminogen activator-loaded echogenic liposomes J. Drug Target. 15 2007 109 114
90. S.T. Laing, M. Moody, B. Smulevitz, H. Kim, P. Kee, S.L. Huang, C.K. Holland, and D.D. McPherson Ultrasound-enhanced thrombolytic effect of tissue plasminogen activator-loaded echogenic liposomes in an in vivo rabbit aorta thrombus model: brief report Arterioscler. Thromb. Vasc. Biol. 31 2011 1357 1359
91. S.T. Laing, M.R. Moody, H. Kim, B. Smulevitz, S.L. Huang, C.K. Holland, D.D. McPherson, and M.E. Klegerman Thrombolytic efficacy of tissue plasminogen activator-loaded echogenic liposomes in a rabbit thrombus model Thromb. Res. 130 2012 629 635
92. G.J. Shaw, J.M. Meunier, S.L. Huang, C.J. Lindsell, D.D. McPherson, and C.K. Holland Ultrasound-enhanced thrombolysis with tPA-loaded echogenic liposomes Thromb. Res. 124 2009 306 310
93. D.A.B. Smith, S.S. Vaidya, J.A. Kopechek, S.L. Huang, M.E. Klegerman, D.D. McPherson, and C.K. Holland Ultrasound-triggered release of recombinant tissue-type plasminogen activator from echogenic liposomes Ultrasound Med. Biol. 36 2010 145 157
94. S. Erdogan, A.Y. Ozer, and H. Bilgili In vivo behaviour of vesicular urokinase Int. J. Pharm. 295 2005 1 6
95. X.T. Wang, S. Li, X.B. Zhang, and X.P. Hou Preparation of thrombus-targeted urokinase liposomes and its thrombolytic effect in model rats Acta Pharm. Sin. 38 2003 231 235
96. H. Bounameaux, P. Cirafici, P. deMoerloose, P.A. Schneider, D. Slosman, G. Reber, and P.F. Unger Measurement of D-dimer in plasma as diagnostic aid in suspected pulmonary embolism Lancet 337 1991 196 200
97. C.P. Lu, H. Yang, J. Wang, and X.L. Dong Thrombolysis of rabbit's pulmonary embolism with thrombus-targeted urokinase immune liposome Chin. J. Cardiol. 37 2009 1035 1038
98. S. Vanderschueren, L. Stockx, G. Wilms, H. Lacroix, R. Verhaeghe, J. Vermylen, and D. Collen Thrombolytic therapy of peripheral arterial occlusion with recombinant staphylokinase Circulation 92 1995 2050 2057
99. L. Yang, C.H. Shi, Y.Y. Chang, H. Li, P. Xiao, W.Z. Yang, and Q. Zeng Entrapment of recombinant staphylokinase by liposomes: formulations, preparation, characterization and behavior in vivo J. Drug Deliv. Sci. Technol. 18 2008 245 251
100. L. Li, T.L.M. ten Hagen, D. Schipper, T.M. Wijnberg, G.C. van Rhoon, A.M.M. Eggermont, L.H. Lindner, and G.A. Koning Triggered content release from optimized stealth thermosensitive liposomes using mild hyperthermia J. Control. Release 143 2010 274 279
101. D. Needham, and M.W. Dewhirst The development and testing of a new temperature-sensitive drug delivery system for the treatment of solid tumors Adv. Drug Deliv. Rev. 53 2001 285 305
102. V. Saxena, C.G. Johnson, A.H. Negussie, K.V. Sharma, M.R. Dreher, and B.J. Wood Temperature-sensitive liposome-mediated delivery of thrombolytic agents Int. J. Hyperth. 31 2015 67 73
103. V.J. Marder, K. Landskroner, V. Novokhatny, T.P. Zimmerman, M. Kong, J.J. Kanouse, and G. Jesmok Plasmin induces local thrombolysis without causing hemorrhage: a comparison with tissue plasminogen activator in the rabbit Thromb. Haemost. 86 2001 739 745
104. V.J. Marder, D.J. Chute, S. Starkman, A.M. Abolian, C. Kidwell, D. Liebeskind, B. Ovbiagele, F. Vinuela, G. Duckwiler, R. Jahan, P.M. Vespa, S. Selco, V. Rajajee, D. Kim, N. Sanossian, and J.L. Saver Analysis of thrombi retrieved from cerebral arteries of patients with acute ischemic stroke Stroke 37 2006 2086 2093
105. R.D. Shlansky-Goldberg, A.H. Matsumoto, G.A. Baumbach, J.B. Siegel, R.D. Raabe, T.P. Murphy, C. Deng, J.R. Dawkins, and V.J. Marder A first-in-human phase I trial of locally delivered human plasmin for hemodialysis graft occlusion J. Thromb. Haemost. 6 2008 944 950
106. M.A. Kandadai, J.M. Meunier, K. Hart, C.K. Holland, and G.J. Shaw Plasmin-loaded echogenic liposomes for ultrasound-mediated thrombolysis Transl. Stroke Res. 6 2015 78 87
107. S. Absar, N. Gupta, K. Nahar, and F. Ahsan Engineering plasminoge acivators for targeting thrombus and heightening thrombolytic efficacy J. Thromb. Haemost. 13 2015 1545 1556
108. S.M. Janib, A.S. Moses, and J.A. Mackay Imaging and drug delivery using theranostic nanoparticles Adv. Drug Deliv. Rev. 62 2010 1052 1063
109. P. Wust, B. Hildebrandt, G. Sreenivasa, B. Rau, J. Gellermann, H. Riess, R. Felix, and P.M. Schlag Hyperthermia in combined treatment of cancer Lancet Oncol. 3 2002 487 497