Tissue plasminogen activator-based nanothrombolysis for ischemic stroke

References

• Mozaffarian D, Benjamin EJ, Go AS, et al. Heart disease and stroke statistics–2015 update: a report from the American Heart Association. Circulation. 2015 Jan;131(4):e29–322.
   PubMed Web of Science ®Google Scholar
• Bivard A, Lin L, Parsonsb MW. Review of stroke thrombolytics. J Stroke. 2013 May;15(2):90–98.
   PubMed Web of Science ®Google Scholar
• Marshall RS. Progress in intravenous thrombolytic therapy for acute stroke. JAMA Neurol. 2015 Aug;72(8):928–934.
   PubMed Web of Science ®Google Scholar
• Chevilley A, Lesept F, Lenoir S, et al. Impacts of tissue-type plasminogen activator (tPA) on neuronal survival. Front Cell Neurosci. 2015;9:415.
   PubMed Web of Science ®Google Scholar
• Wallén P, Bergsdorf N, Rånby M. Purification and identification of two structural variants of porcine tissue plasminogen activator by affinity adsorption on fibrin. Biochim Biophys Acta. 1982 Nov;719(2):318–328.
   PubMedGoogle Scholar
• Ichinose A, Kisiel W, Fujikawa K. Proteolytic activation of tissue plasminogen activator by plasma and tissue enzymes. FEBS Lett. 1984 Oct 01;175(2):412–418.
   PubMed Web of Science ®Google Scholar
• Bhattacharjee P, Bhattacharyya D. An insight into the abnormal fibrin clots — its pathophysiological roles. In Fibrinolysis and Thrombolysis. Krasimir Kolev (Ed). Rijeka: InTech; 2014. Ch. 0.
   Google Scholar
• Collen D. Molecular mechanisms of fibrinolysis and their application to fibrin-specific thrombolytic therapy. J Cell Biochem. 1987 Feb;33(2):77–86.
   PubMed Web of Science ®Google Scholar
• Yepes M, Sandkvist M, Moore EG, et al. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest. 2003 Nov;112(10):1533–1540.
   PubMed Web of Science ®Google Scholar
• Joshi MD. Advances in nanomedicine for treatment of stroke. Int J Nanomedicine Nanosurgery. 2016 May; 2(3). doi 10.16966/2470-3206.113.
   PubMedGoogle Scholar
• Kidwell CS, Latour L, Saver JL, et al. Thrombolytic toxicity: blood brain barrier disruption in human ischemic stroke. Cerebrovasc Dis. 2008;25(4):338–343.
   PubMed Web of Science ®Google Scholar
• Yepes M, Roussel BD, Ali C, et al. Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic. Trends Neurosci. 2009 Jan;32(1):48–55.
   PubMed Web of Science ®Google Scholar
• Polavarapu R, Gongora MC, Yi H, et al. Tissue-type plasminogen activator-mediated shedding of astrocytic low-density lipoprotein receptor-related protein increases the permeability of the neurovascular unit. Blood. 2007 Apr 15;109(8):3270–3278.
   PubMed Web of Science ®Google Scholar
• Su EJ, Fredriksson L, Geyer M, et al. Activation of PDGF-CC by tissue plasminogen activator impairs blood-brain barrier integrity during ischemic stroke. Nat Med. 2008 Jul;14(7):731–737.
   PubMed Web of Science ®Google Scholar
• Haile WB, Wu J, Echeverry R, et al. Tissue-type plasminogen activator has a neuroprotective effect in the ischemic brain mediated by neuronal TNF-alpha. J Cereb Blood Flow Metab. 2012 Jan;32(1):57–69.
   PubMed Web of Science ®Google Scholar
• Jeanneret V, Yepes M. The plasminogen activation system promotes dendritic spine recovery and improvement in neurological function after an ischemic stroke. Transl Stroke Res. 2017 Feb; 8(1):47–56.
   Web of Science ®Google Scholar
• Bertrand T, Lesept F, Chevilley A, et al. Conformations of tissue plasminogen activator (tPA) orchestrate neuronal survival by a crosstalk between EGFR and NMDAR. Cell Death Dis. 2015 Oct;15(6):e1924.
   Google Scholar
• Lemarchand E, Maubert E, Haelewyn B, et al. Stressed neurons protect themselves by a tissue-type plasminogen activator-mediated EGFR-dependent mechanism. Cell Death Differ. 2016 Jan;23(1):123–131.
   PubMed Web of Science ®Google Scholar
• Lemarchant S, Docagne F, Emery E, et al. tPA in the injured central nervous system: different scenarios starring the same actor? Neuropharmacology. 2012 Feb;62(2):749–756.
   PubMed Web of Science ®Google Scholar
• Lee TW, Tsang VW, Birch NP. Physiological and pathological roles of tissue plasminogen activator and its inhibitor neuroserpin in the nervous system. Front Cell Neurosci. 2015;9:396.
   PubMed Web of Science ®Google Scholar
• Fredriksson L, Lawrence DA, Medcalf RL. tPA modulation of the blood–brain barrier: a unifying explanation for the pleiotropic effects of tPA in the CNS. Semin Thromb Hemost. 2017 03 02;43(2):154–168.
   PubMed Web of Science ®Google Scholar
• Grummisch JA, Jadavji NM, Smith PD. The pleiotropic effects of tissue plasminogen activator in the brain: implications for stroke recovery. Neural Regen Res. 2016 Jan 09;11(9):1401–1402.
   PubMed Web of Science ®Google Scholar
• Kim JY, Kim JK, Park JS, et al. The use of PEGylated liposomes to prolong circulation lifetimes of tissue plasminogen activator. Biomaterials. 2009 Oct;30(29):5751–5756.
   PubMed Web of Science ®Google Scholar
• Asahi M, Rammohan R, Sumii T, et al. Antiactin-targeted immunoliposomes ameliorate tissue plasminogen activator-induced hemorrhage after focal embolic stroke. J Cereb Blood Flow Metab. 2003 Aug;23(8):895–899.
   PubMed Web of Science ®Google Scholar
• Absar S, Nahar K, Kwon YM, et al. Thrombus-targeted nanocarrier attenuates bleeding complications associated with conventional thrombolytic therapy. Pharm Res. 2013 Jun;30(6):1663–1676.
   PubMed Web of Science ®Google Scholar
• Chung TW, Wang SS, Tsai WJ. Accelerating thrombolysis with chitosan-coated plasminogen activators encapsulated in poly-(lactide-co-glycolide) (PLGA) nanoparticles. Biomaterials. 2008 Jan;29(2):228–237.
   PubMed Web of Science ®Google Scholar
• Korin N, Kanapathipillai M, Matthews BD, et al. Shear-activated nanotherapeutics for drug targeting to obstructed blood vessels. Science. 2012 Aug;337(6095):738–742.
   PubMed Web of Science ®Google Scholar
• Park Y, Liang J, Yang Z, et al. Controlled release of clot-dissolving tissue-type plasminogen activator from a poly(L-glutamic acid) semi-interpenetrating polymer network hydrogel. J Control Release. 2001 Jul;75(1–2):37–44.
   PubMed Web of Science ®Google Scholar
• Uesugi Y, Kawata H, Jo J, et al. An ultrasound-responsive nano delivery system of tissue-type plasminogen activator for thrombolytic therapy. J Control Release. 2010 Oct;147(2):269–277.
   PubMed Web of Science ®Google Scholar
• Chen J-P, Yang P-C, Ma Y-H, et al. Characterization of chitosan magnetic nanoparticles for in situ delivery of tissue plasminogen activator. Carbohydr Polym. 2011 2 11;84(1):364–372.
   Web of Science ®Google Scholar
• Kempe M, Kempe H, Snowball I, et al. The use of magnetite nanoparticles for implant-assisted magnetic drug targeting in thrombolytic therapy. Biomaterials. 2010 Dec;31(36):9499–9510.
   PubMed Web of Science ®Google Scholar
• Silva AKA, Luciani N, Gazeau F, et al. Combining magnetic nanoparticles with cell derived microvesicles for drug loading and targeting. Nanomedicine: Nanotechnology, Biol Med. 2015 4;11(3):645–655.
   PubMed Web of Science ®Google Scholar
• Voros E, Cho M, Ramirez M, et al. TPA immobilization on iron oxide nanocubes and localized magnetic hyperthermia accelerate blood clot lysis. Adv Funct Mater. 2015;25(11):1709–1718.
   Web of Science ®Google Scholar
• Yan W-C, Chua QW, Ong XJ, et al. Fabrication of ultrasound-responsive microbubbles via coaxial electrohydrodynamic atomization for triggered release of tPA. J Colloid Interface Sci. 2017 09 01;501:282–293.
   PubMed Web of Science ®Google Scholar
• Tiukinhoy-Laing SD, Huang S, Klegerman M, et al. Ultrasound-facilitated thrombolysis using tissue-plasminogen activator-loaded echogenic liposomes. Thromb Res. 2007;119(6):777–784.
   PubMed Web of Science ®Google Scholar
• Hagisawa K, Nishioka T, Suzuki R, et al. Thrombus-targeted perfluorocarbon-containing liposomal bubbles for enhancement of ultrasonic thrombolysis: in vitro and in vivo study. J Thromb Haemost. 2013 Aug;11(8):1565–1573.
   PubMed Web of Science ®Google Scholar
• Kandadai MA, Mukherjee P, Shekhar H, et al. Microfluidic manufacture of rt-PA -loaded echogenic liposomes. Biomed Microdevices. 2016 Jun;18(3):48.
   PubMed Web of Science ®Google Scholar
• Absar S, Choi S, Yang VC, et al. Heparin-triggered release of camouflaged tissue plasminogen activator for targeted thrombolysis. J Control Release. 2012 Jan;157(1):46–54.
   PubMed Web of Science ®Google Scholar
• Absar S, Kwon YM, Ahsan F. Bio-responsive delivery of tissue plasminogen activator for localized thrombolysis. J Control Release. 2014 Mar;177:42–50.
   PubMed Web of Science ®Google Scholar
• Heeremans JL, Gerritsen HR, Meusen SP, et al. The preparation of tissue-type Plasminogen Activator (t-PA) containing liposomes: entrapment efficiency and ultracentrifugation damage. J Drug Target. 1995;3(4):301–310.
   PubMed Web of Science ®Google Scholar
• Heeremans JL, Prevost R, Bekkers ME, et al. Thrombolytic treatment with tissue-type plasminogen activator (t-PA) containing liposomes in rabbits: a comparison with free t-PA. Thromb Haemost. 1995 Mar;73(3):488–494.
   PubMed Web of Science ®Google Scholar
• Lanza GM, Marsh JN, Hu G, et al. Rationale for a nanomedicine approach to thrombolytic therapy. Stroke. 2010 Oct;41(10 Suppl):S42–4.
   PubMed Web of Science ®Google Scholar
• Soeda S, Kakiki M, Shimeno H, et al. Some properties of tissue-type plasminogen activator reconstituted onto phospholipid and/or glycolipid vesicles. Biochem Biophys Res Commun. 1987 Jul;146(1):94–100.
   PubMed Web of Science ®Google Scholar
• Koudelka S, Mikulik R, Mašek J, et al. Liposomal nanocarriers for plasminogen activators. J Control Release. 2016 Apr;227:45–57.
   PubMed Web of Science ®Google Scholar
• Ware S, Donahue JP, Hawiger J, et al. Structure of the fibrinogen gamma-chain integrin binding and factor XIIIa cross-linking sites obtained through carrier protein driven crystallization. Protein Sci. 1999 Dec;8(12):2663–2671.
   PubMed Web of Science ®Google Scholar
• Wang SS, Chou NK, Chung TW. The t-PA-encapsulated PLGA nanoparticles shelled with CS or CS-GRGD alter both permeation through and dissolving patterns of blood clots compared with t-PA solution: an in vitro thrombolysis study. J Biomed Mater Res A. 2009 Dec;91(3):753–761.
   PubMedGoogle Scholar
• Uesugi Y, Kawata H, Saito Y, et al. Ultrasound-responsive thrombus treatment with zinc-stabilized gelatin nano-complexes of tissue-type plasminogen activator. J Drug Target. 2012 Apr;20(3):224–234.
   PubMed Web of Science ®Google Scholar
• Tran PH, Tran TT, Vo TV, et al. Promising iron oxide-based magnetic nanoparticles in biomedical engineering. Arch Pharm Res. 2012 Dec;35(12):2045–2061.
   PubMed Web of Science ®Google Scholar
• Castellanos-Rubio I, Insausti M, de Muro I, et al. The impact of the chemical synthesis on the magnetic properties of intermetallic PdFe nanoparticles. J Nanoparticle Res. 2015 MAY 22;17(5).
   Web of Science ®Google Scholar
• Wu W, Wu Z, Yu T, et al. Recent progress on magnetic iron oxide nanoparticles: synthesis, surface functional strategies and biomedical applications. Sci Technol Adv Mater. 2015 Apr;16(2):023501.
   PubMed Web of Science ®Google Scholar
• Ma YH, Wu SY, Wu T, et al. Magnetically targeted thrombolysis with recombinant tissue plasminogen activator bound to polyacrylic acid-coated nanoparticles. Biomaterials. 2009 Jul;30(19):3343–3351.
   PubMed Web of Science ®Google Scholar
• Chen JP, Yang PC, Ma YH, et al. Superparamagnetic iron oxide nanoparticles for delivery of tissue plasminogen activator. J Nanosci Nanotechnol. 2011 Dec;11(12):11089–11094.
   PubMed Web of Science ®Google Scholar
• Chen JP, Yang PC, Ma YH, et al. Targeted delivery of tissue plasminogen activator by binding to silica-coated magnetic nanoparticle. Int J Nanomedicine. 2012;7:5137–5149.
   PubMed Web of Science ®Google Scholar
• Yang HW, Hua MY, Lin KJ, et al. Bioconjugation of recombinant tissue plasminogen activator to magnetic nanocarriers for targeted thrombolysis. Int J Nanomedicine. 2012;7:5159–5173.
   PubMed Web of Science ®Google Scholar
• Tadayon A, Jamshidi R, Esmaeili A. Targeted thrombolysis of tissue plasminogen activator and streptokinase with extracellular biosynthesis nanoparticles using optimized Streptococcus equi supernatant. Int J Pharm. 2016 Mar 30; 501(1–2):300–310.
   PubMedGoogle Scholar
• Hu J, Huang W, Huang S, et al. Magnetically active Fe3O4 nanorods loaded with tissue plasminogen activator for enhanced thrombolysis. Nano Research. 2016 Sep;9(9):2652–2661.
   Web of Science ®Google Scholar
• Meairs S. Sonothrombolysis. Front Neurol Neurosci. 2015;36:83–93.
   PubMedGoogle Scholar
• Francis CW, Blinc A, Lee S, et al. Ultrasound accelerates transport of recombinant tissue plasminogen activator into clots. Ultrasound Med Biol. 1995;21(3):419–424.
   PubMed Web of Science ®Google Scholar
• Siddiqi F, Blinc A, Braaten J, et al. Ultrasound increases flow through fibrin gels. Thromb Haemost. 1995 Mar;73(3):495–498.
   PubMed Web of Science ®Google Scholar
• Cwf MD. Ultrasound-enhanced thrombolysis. Echocardiography. 2001;18(3):239–246.
   PubMed Web of Science ®Google Scholar
• de Saint Victor M, Crake C, Coussios CC, et al. Properties, characteristics and applications of microbubbles for sonothrombolysis. Expert Opin Drug Deliv. 2014 Feb;11(2):187–209.
   PubMed Web of Science ®Google Scholar
• Alexandrov AV, Demchuk AM, Felberg RA, et al. High rate of complete recanalization and dramatic clinical recovery during tPA infusion when continuously monitored with 2-MHz transcranial Doppler monitoring. Stroke. 2000 Mar;31(3):610–614.
   PubMed Web of Science ®Google Scholar
• Alexandrov AV, Molina CA, Grotta JC, et al. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. N Engl J Med. 2004 Nov;351(21):2170–2178.
   PubMed Web of Science ®Google Scholar
• Eggers J, Koch B, Meyer K, et al. Effect of ultrasound on thrombolysis of middle cerebral artery occlusion. Ann Neurol. 2003 Jun;53(6):797–800.
   PubMed Web of Science ®Google Scholar
• Daffertshofer M, Gass A, Ringleb P, et al. Transcranial low-frequency ultrasound-mediated thrombolysis in brain ischemia: increased risk of hemorrhage with combined ultrasound and tissue plasminogen activator: results of a phase II clinical trial. Stroke. 2005 Jul;36(7):1441–1446.
   PubMed Web of Science ®Google Scholar
• El-Sherbiny IM, Elkholi IE, Yacoub MH. Tissue plasminogen activator-based clot busting: controlled delivery approaches. Glob Cardiol Sci Pract. 2014;2014(3):336–349.
   PubMedGoogle Scholar
• Molina CA, Ribo M, Rubiera M, et al. Microbubble administration accelerates clot lysis during continuous 2-MHz ultrasound monitoring in stroke patients treated with intravenous tissue plasminogen activator. Stroke. 2006 Feb;37(2):425–429.
   PubMed Web of Science ®Google Scholar
• Everbach EC, Francis CW. Cavitational mechanisms in ultrasound-accelerated thrombolysis at 1 MHz. Ultrasound Med Biol. 2000 Sep;26(7):1153–1160.
   PubMed Web of Science ®Google Scholar
• Dijkmans PA, Juffermans LJ, Musters RJ, et al. Microbubbles and ultrasound: from diagnosis to therapy. Eur J Echocardiogr. 2004 Aug;5(4):245–256.
   PubMedGoogle Scholar
• Unger EC, Porter T, Culp W, et al. Therapeutic applications of lipid-coated microbubbles. Adv Drug Deliv Rev. 2004 May;56(9):1291–1314.
   PubMed Web of Science ®Google Scholar
• Hua X, Liu P, Gao Y-H, et al. Construction of thrombus-targeted microbubbles carrying tissue plasminogen activator and their in vitro thrombolysis efficacy: a primary research. J Thromb Thrombolysis. 2010 07 01;30(1):29–35.
   PubMed Web of Science ®Google Scholar
• Hua X, Zhou L, Liu P, et al. In vivo thrombolysis with targeted microbubbles loading tissue plasminogen activator in a rabbit femoral artery thrombus model. J Thromb Thrombolysis. 2014 07 01;38(1):57–64.
   PubMed Web of Science ®Google Scholar
• Yan W-C, Ong XJ, Pun KT, et al. Preparation of tPA-loaded microbubbles as potential theranostic agents: a novel one-step method via coaxial electrohydrodynamic atomization technique. Chem Eng J. 2017 01 01;307:168–180.
   Web of Science ®Google Scholar
• Smith DA, Vaidya SS, Kopechek JA, et al. Ultrasound-triggered release of recombinant tissue-type plasminogen activator from echogenic liposomes. Ultrasound Med Biol. 2010 Jan;36(1):145–157.
   PubMed Web of Science ®Google Scholar
• Huang SL. Liposomes in ultrasonic drug and gene delivery. Adv Drug Deliv Rev. 2008 Jun;60(10):1167–1176.
   PubMed Web of Science ®Google Scholar
• Smith DAB, Vaidya S, Kopechek JA, et al. Echogenic liposomes loaded with recombinant tissue‐type plasminogen activator (rt‐PA) for image‐guided, ultrasound‐triggered drug release. J Acoust Soc Am. 2008;122(5). doi: 10.1121/1.2942738
   Google Scholar
• Shekhar H, Bader KB, Huang S, et al. In vitro thrombolytic efficacy of echogenic liposomes loaded with tissue plasminogen activator and octafluoropropane gas. Phys Med Biol. 2016 Dec;62(2):517–538.
   PubMed Web of Science ®Google Scholar
• Shaw GJ, Meunier JM, Huang SL, et al. Ultrasound-enhanced thrombolysis with tPA-loaded echogenic liposomes. Thromb Res. 2009 Jul;124(3):306–310.
   PubMed Web of Science ®Google Scholar
• Tiukinhoy-Laing SD, Buchanan K, Parikh D, et al. Fibrin targeting of tissue plasminogen activator-loaded echogenic liposomes. J Drug Target. 2007 Feb;15(2):109–114.
   PubMed Web of Science ®Google Scholar
• Klegerman ME, Zou Y, McPherson DD. Fibrin targeting of echogenic liposomes with inactivated tissue plasminogen activator. J Liposome Res. 2008;18(2):95–112.
   PubMed Web of Science ®Google Scholar
• Laing ST, Moody MR, Kim H, et al. Thrombolytic efficacy of tissue plasminogen activator-loaded echogenic liposomes in a rabbit thrombus model. Thromb Res. 2012 10;130(4):629–635.
   PubMed Web of Science ®Google Scholar
• Absar S, Choi S, Ahsan F, et al. Preparation and characterization of anionic oligopeptide-modified tissue plasminogen activator for triggered delivery: an approach for localized thrombolysis. Thromb Res. 2013 Mar;131(3):e91–9.
   PubMed Web of Science ®Google Scholar
• Bahadar H, Maqbool F, Niaz K, et al. Toxicity of nanoparticles and an overview of current experimental models. Iran Biomed J. 2016;20(1):1–11.
   PubMedGoogle Scholar
• Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron. 2010 Jul;67(2):181–198.
   Web of Science ®Google Scholar
• Sicard KM, Fisher M. Animal models of focal brain ischemia. Exp Transl Stroke Med. 2009 Nov;13(1):7.
   Google Scholar
• Liang LJ, Yang JM, Jin XC. Cocktail treatment, a promising strategy to treat acute cerebral ischemic stroke? Med Gas Res. 2016 Mar;6(1):33–38.
   PubMed Web of Science ®Google Scholar
• Murata Y, Rosell A, Scannevin RH, et al. Extension of the thrombolytic time window with minocycline in experimental stroke. Stroke. 2008 Dec;39(12):3372–3377.
   PubMed Web of Science ®Google Scholar
• Li M, Zhang Z, Sun W, et al. 17β-estradiol attenuates breakdown of blood-brain barrier and hemorrhagic transformation induced by tissue plasminogen activator in cerebral ischemia. Neurobiol Dis. 2011 Dec;44(3):277–283.
   PubMed Web of Science ®Google Scholar
• Fukuta T, Asai T, Yanagida Y, et al. Combination therapy with liposomal neuroprotectants and tissue plasminogen activator for treatment of ischemic stroke. Faseb J. 2017;31(5):1879–1890.
   PubMed Web of Science ®Google Scholar
• Lee HJ, Park J, Yoon OJ, et al. Amine-modified single-walled carbon nanotubes protect neurons from injury in a rat stroke model. Nat Nano. 2011 02;6(2):121–125. print.
   PubMed Web of Science ®Google Scholar
• Higgins P, Dawson J, Walters M. Nanomedicine: nanotubes reduce stroke damage. Nat Nanotechnol. 2011;83–84. England.
   PubMed Web of Science ®Google Scholar
• Rabinstein AA. Stroke in 2015: acute endovascular recanalization therapy comes of age. ‎Nat Rev Neurol. 2016;12:67–68.
   PubMed Web of Science ®Google Scholar