Skip to main content

Advertisement

Log in

Progress of nanomaterials in the treatment of thrombus

  • Review Article
  • Published:
Drug Delivery and Translational Research Aims and scope Submit manuscript

Abstract

Thrombus has long been the major contributor of death and disability because it can cause adverse effects to varying degrees on the body, resulting in vascular blockage, embolism, heart valve deformation, widespread bleeding, etc. However, clinically, conventional thrombolytic drug treatments have hemorrhagic complication risks and easy to miss the best time of treatment window. Thus, it is an urgent need to investigate newly alternative treatment strategies that can reduce adverse effects and improve treatment effectiveness. Drugs based on nanomaterials act as a new biomedical strategy and promising tools, and have already been investigated for both diagnostic and therapeutic purposes in thrombus therapy. Recent studies have some encouraging progress. In the present review, we primarily concern with the latest developments in the areas of nanomedicines targeting thrombosis therapy. We present the thrombus’ formation, characteristics, and biomarkers for diagnosis, overview recent emerging nanomedicine strategies for thrombus therapy, and focus on the future design directions, challenges, and prospects in the nanomedicine application in thrombus therapy.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of data and materials

No new datasets were collected or generated for the purposes of this review article.

Abbreviations

CVD:

Cardiovascular disease

NPs:

Nanoparticles

US:

Ultrasound

PE:

Pulmonary embolism

FXIIIa:

Fibrin and activating factor XIII

PC:

Phosphatidylcholine

GPIIb/IIIa:

Glycoprotein IIb/IIIa

RGD:

Arg–Gly–Asp

PDI:

Protein disulfide isomerase

ERp57:

Endoplasmic Recombinant protein 57

LDL:

Low-density lipoprotein

PSGL-1:

P-selectin glycoprotein ligand 1

RGDS:

Arg–Gly–Asp–Ser

KQAGDV:

Lys–Gln–Ala–Gly–Asp–Val

CREKA:

Cysteine–arginine–glutamate–lysine–alanine

PPACK:

Phenylalanine–proline–arginine–chloromethylketone

ROS:

Reactive oxygen species

HOCl:

Hypochlorous acid

Nox:

NADPH oxidase family

SS-NPA:

Shear-sensitive nanoparticle aggregates

SK:

Streptokinase

PEG:

Polyethylene glycol

ICCA:

1-(4-Isopropylphenyl)-β-carboline-3-carboxylic acid

THC:

1,2,3,4-Tetrahydro-β-carbinol

THCMA:

3S-THC-3-methyl aspartyl ester

LIFU:

Low-intensity focused ultrasound

NPep:

Nano emulsion

EDC/NHS:

1-Ethyl-3-(3-dimethylaminopropyl) carbodiimide/N-hydroxysuccinimide

EPR effect:

Enhanced permeability and retention effect

cRGD:

Cyclo(Arg–Gly–Asp–d-Phe–Cys)

UK:

Urokinase

UV:

Ultraviolet light

UCNPs:

Upconversion nanomaterials

NIR:

Near infrared light

Azo:

Azobenzene

PDA:

Polydopamine

HMSN:

Hollow mesoporous silica

Nets:

Networks

Cur:

Curcumin

HA:

Hyaluronic acid

PVAX:

Poly(vanillyl alcohol-oxalate copolymer)

VA:

Vanillyl alcohol

Oxd:

Oxidized dextran

PM:

Platelet membranes

DTX:

Doxorubicin

PMP:

Platelet granules

PS:

Phosphatidylserine

ECS:

Extracellular space

FDA:

U.S. Food and Drug Administration

References

  1. Zenych A, Fournier L, Chauvierre C. Nanomedicine progress in thrombolytic therapy. Biomaterials. 2020;258:120297.

  2. Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med. 2006;3(11):e442.

  3. Lutsey PL, Zakai NA. Epidemiology and prevention of venous thromboembolism. Nat Rev Cardiol. 2023;20(4):248–62.

    Article  PubMed  Google Scholar 

  4. Correa-Paz C, da Silva-Candal A, Polo E, Parcq J, Vivien D, Maysinger D, et al. New approaches in nanomedicine for ischemic stroke. Pharmaceutics. 2021;13(5).

  5. Wang Y, Pisapati AV, Zhang XF, Cheng X. Recent developments in nanomaterial-based shear-sensitive drug delivery systems. Adv Healthc Mater. 2021;10(13):e2002196.

  6. Ma H, Jiang Z, Xu J, Liu J, Guo ZN. Targeted nano-delivery strategies for facilitating thrombolysis treatment in ischemic stroke. Drug Deliv. 2021;28(1):357-71.

  7. Zhu J, Wang J, Li Y. Recent advances in magnetic nanocarriers for tumor treatment. Biomed Pharmacother. 2023;159.

    Article  CAS  PubMed  Google Scholar 

  8. Song D, Li C, Zhu M, Chi S, Liu Z. Tracking hepatic ischemia-reperfusion injury in real time with a reversible NIR-IIb fluorescent redox probe. Angew Chem Int Ed Engl. 2022;61(44).

    Article  CAS  PubMed  Google Scholar 

  9. Cabrera D, Eizadi Sharifabad M, Ranjbar JA, Telling ND, Harper AGS. Clot-targeted magnetic hyperthermia permeabilizes blood clots to make them more susceptible to thrombolysis. J Thromb Haemost. 2022;20(11):2556–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Yu W, Yin N, Yang Y, Xuan C, Liu X, Liu W, et al. Rescuing ischemic stroke by biomimetic nanovesicles through accelerated thrombolysis and sequential ischemia-reperfusion protection. Acta Biomater. 2022;140:625–40.

    Article  CAS  PubMed  Google Scholar 

  11. Shen M, Wang Y, Hu F, Lv L, Chen K, Xing G. Thrombolytic agents: nanocarriers in targeted release. Molecules (Basel, Switzerland). 2021;26(22):6776.

    Article  CAS  PubMed  Google Scholar 

  12. Furie B, Furie BC. Mechanisms of thrombus formation. N Engl J Med. 2008;359(9):938–49.

    Article  CAS  PubMed  Google Scholar 

  13. De Maeseneer MG, Kakkos SK, Aherne T, Baekgaard N, Black S, Blomgren L, et al. Editor's choice - European Society for Vascular Surgery (ESVS) 2022 clinical practice guidelines on the management of chronic venous disease of the lower limbs. Eur J Vasc Endovasc Surg. 2022;63(2):184–267.

    Article  PubMed  Google Scholar 

  14. Manz XD, Bogaard HJ, Aman J. Regulation of VWF (von Willebrand factor) in inflammatory thrombosis. Arterioscler Thromb Vasc Biol. 2022;42(11):1307–20.

    Article  CAS  PubMed  Google Scholar 

  15. Bettiol A, Alibaz-Oner F, Direskeneli H, Hatemi G, Saadoun D, Seyahi E, et al. Vascular Behcet syndrome: from pathogenesis to treatment. Nat Rev Rheumatol. 2023;19(2):111–26.

    Article  CAS  PubMed  Google Scholar 

  16. Zhou S, Zhao W, Hu J, Mao C, Zhou M. Application of nanotechnology in thrombus therapy. Adv Healthc Mater. 2023;12(7).

    Article  PubMed  Google Scholar 

  17. Dou H, Kotini A, Liu W, Fidler T, Endo-Umeda K, Sun X, et al. Oxidized phospholipids promote netosis and arterial thrombosis in LNK(SH2B3) deficiency. Circulation. 2021;144(24):1940–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Alkarithi G, Duval C, Shi Y, Macrae FL, Ariens RAS. Thrombus structural composition in cardiovascular disease. Arterioscler Thromb Vasc Biol. 2021;41(9):2370–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Adrover JM, Pellico J, Fernández-Barahona I, Martín-Salamanca S, Ruiz-Cabello J, Hidalgo A, et al. Thrombo-tag, an in vivo formed nanotracer for the detection of thrombi in mice by fast pre-targeted molecular imaging. Nanoscale. 2020;12(45):22978–87.

    Article  CAS  PubMed  Google Scholar 

  20. Klaeske K, Meyer AL, Saeed D, Eifert S, Jawad K, Sieg F, et al. Decreased platelet specific receptor expression of P-selectin and GPIIb/IIIa predict future non-surgical bleeding in patients after left ventricular assist device implantation. Int J Mol Sci. 2022;23(18).

  21. Bachelet L, Bertholon I, Lavigne D, Vassy R, Jandrot-Perrus M, Chaubet F, et al. Affinity of low molecular weight fucoidan for p-selectin triggers its binding to activated human platelets. Biochem Biophys Acta. 2009;1790(2):141–6.

    Article  CAS  PubMed  Google Scholar 

  22. Nayak L, Sweet DR, Thomas A, Lapping SD, Kalikasingh K, Madera A, et al. A targetable pathway in neutrophils mitigates both arterial and venous thrombosis. Sci Transl Med. 2022;14(660):eabj7465.

  23. Hajtuch J, Iwicka E, Szczoczarz A, Flis D, Megiel E, Cieciorski P, et al. The pharmacological effects of silver nanoparticles functionalized with eptifibatide on platelets and endothelial cells. Int J Nanomedicine. 2022;17:4383–400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Yin R, Zhou L, Gao N, Lin L, Sun H, Chen D, et al. Unveiling the disaccharide-branched glycosaminoglycan and anticoagulant potential of its derivatives. Biomacromol. 2021;22(3):1244–55.

    Article  CAS  Google Scholar 

  25. Zhou XH, Cheng ZP, Lu M, Lin WY, Luo LL, Ming ZY, et al. Adiponectin receptor agonist adiporon modulates human and mouse platelet function. Acta Pharmacol Sin. 2023;44(2):356–66.

    Article  CAS  PubMed  Google Scholar 

  26. Souri M, Yokoyama C, Osaki T, Ichinose A. Antibodies against noncatalytic b subunit of factor XIII inhibit activation of factor XIII and fibrin crosslinking. Thromb Haemost. 2023;123(9):841–54.

    Article  PubMed  Google Scholar 

  27. Pasternack R, Buchold C, Jahnig R, Pelzer C, Sommer M, Heil A, et al. Novel inhibitor ZED3197 as potential drug candidate in anticoagulation targeting coagulation FXIIIa (F13a). J Thromb Haemost. 2020;18(1):191–200.

    Article  CAS  PubMed  Google Scholar 

  28. Zhang N, Ru B, Hu J, Xu L, Wan Q, Liu W, et al. Recent advances of creka peptide-based nanoplatforms in biomedical applications. J Nanobiotechnology. 2023;21(1):77.

  29. Arjmand S, Pardakhty A, Forootanfar H, Khazaeli P. A road to bring Brij52 back to attention: shear stress sensitive Brij52 niosomal carriers for targeted drug delivery to obstructed blood vessels. Med Hypotheses. 2018;121:137–41.

    Article  CAS  PubMed  Google Scholar 

  30. Behera SS, Pramanik K, Nayak MK. Recent advancement in the treatment of cardiovascular diseases: conventional therapy to nanotechnology. Curr Pharm Des. 2015;21(30):4479–97.

    Article  CAS  PubMed  Google Scholar 

  31. Mohri H, Ohkubo T. How vitronectin binds to activated glycoprotein IIb-IIIa complex and its function in platelet aggregation. Am J Clin Pathol. 1991;96(5):605–9.

    Article  CAS  PubMed  Google Scholar 

  32. Huang J, Li X, Shi X, Zhu M, Wang J, Huang S, et al. Platelet integrin alphaIIbbeta3: signal transduction, regulation, and its therapeutic targeting. J Hematol Oncol. 2019;12(1):26.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Xiong B, Jha V, Min JK, Cho J. Protein disulfide isomerase in cardiovascular disease. Exp Mol Med. 2020;52(3):390–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Juenet M, Aid-Launais R, Li B, Berger A, Aerts J, Ollivier V, et al. Thrombolytic therapy based on fucoidan-functionalized polymer nanoparticles targeting p-selectin. Biomaterials. 2018;156:204–16.

    Article  CAS  PubMed  Google Scholar 

  35. Setiadi H, Yago T, Liu Z, McEver RP. Endothelial signaling by neutrophil-released oncostatin m enhances P-selectin-dependent inflammation and thrombosis. Blood Adv. 2019;3(2):168–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Libby P. The changing landscape of atherosclerosis. Nature. 2021;592(7855):524–33.

    Article  CAS  PubMed  Google Scholar 

  37. Wei Z, Xin G, Wang H, Zheng H, Ji C, Gu J, et al. The diosgenin prodrug nanoparticles with pH-responsive as a drug delivery system uniquely prevents thrombosis without increased bleeding risk. Nanomedicine. 2018;14(3):673–84.

    Article  CAS  PubMed  Google Scholar 

  38. Mitchell JL, Little G, Bye AP, Gaspar RS, Unsworth AJ, Kriek N, et al. Platelet factor XIII-a regulates platelet function and promotes clot retraction and stability. Res Pract Thromb Haemost. 2023;7(5).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Poon C, Gallo J, Joo J, Chang T, Bañobre-López M, Chung EJ. Hybrid, metal oxide-peptide amphiphile micelles for molecular magnetic resonance imaging of atherosclerosis. J Nanobiotechnology. 2018;16(1):92.

  40. Peters D, Kastantin M, Kotamraju VR, Karmali PP, Gujraty K, Tirrell M, et al. Targeting atherosclerosis by using modular, multifunctional micelles. Proc Natl Acad Sci USA. 2009;106(24):9815–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Davie EW, Kulman JD. An overview of the structure and function of thrombin. Semin Thromb Hemost. 2006;32(Suppl 1):3–15.

    Article  CAS  PubMed  Google Scholar 

  42. Gunawan ST, Kempe K, Bonnard T, Cui J, Alt K, Law LS, et al. Multifunctional thrombin-activatable polymer capsules for specific targeting to activated platelets. Adv Mater (Deerfield Beach, Fla). 2015;27(35):5153–7.

  43. Lin KY, Lo JH, Consul N, Kwong GA, Bhatia SN. Self-titrating anticoagulant nanocomplexes that restore homeostatic regulation of the coagulation cascade. ACS Nano. 2014;8(9):8776–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Chen J, Vemuri C, Palekar RU, Gaut JP, Goette M, Hu L, et al. Antithrombin nanoparticles improve kidney reperfusion and protect kidney function after ischemia-reperfusion injury. Am J Physiol Renal Physiol. 2015;308(7):F765–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Tintelnot J, Xu Y, Lesker TR, Schonlein M, Konczalla L, Giannou AD, et al. Microbiota-derived 3-IAA influences chemotherapy efficacy in pancreatic cancer. Nature. 2023;615(7950):168–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Bettiol A, Galora S, Argento FR, Fini E, Emmi G, Mattioli I, et al. Erythrocyte oxidative stress and thrombosis. Expert Rev Mol Med. 2022;24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Braunersreuther V, Montecucco F, Asrih M, Pelli G, Galan K, Frias M, et al. Role of nadph oxidase isoforms Nox1, Nox2 and Nox4 in myocardial ischemia/reperfusion injury. J Mol Cell Cardiol. 2013;64:99–107.

    Article  CAS  PubMed  Google Scholar 

  48. Nabeebaccus AA, Reumiller CM, Shen J, Zoccarato A, Santos CXC, Shah AM. The regulation of cardiac intermediary metabolism by NADPH oxidases. Cardiovasc Res. 2023;118(17):3305–19.

    Article  PubMed  Google Scholar 

  49. Xu H, She P, Ma B, Zhao Z, Li G, Wang Y. Ros responsive nanoparticles loaded with lipid-specific aiegen for atherosclerosis-targeted diagnosis and bifunctional therapy. Biomaterials. 2022;288.

    Article  CAS  PubMed  Google Scholar 

  50. Wang D, Wang X. Diosgenin and its analogs: potential protective agents against atherosclerosis. Drug Des Dev Ther. 2022;16:2305–23.

    Article  Google Scholar 

  51. Li B, Chen R, Zhang Y, Zhao L, Liang H, Yan Y, et al. Rgd modified protein-polymer conjugates for pH-triggered targeted thrombolysis. ACS Appl Bio Mater. 2019;2(1):437–46.

    Article  CAS  PubMed  Google Scholar 

  52. Ferrero JM, Gonzalez-Ascaso A, Matas JFR. The mechanisms of potassium loss in acute myocardial ischemia: new insights from computational simulations. Front Physiol. 2023;14:1074160.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Broersma RJ, Bullemer GD, Mammen EF. Acidosis induced disseminated intravascular microthrombosis and its dissolution by streptokinase. Thromb Diath Haemorrh. 1970;24(1):55–67.

    CAS  PubMed  Google Scholar 

  54. Zhang G, Qin Q, Zhang C, Sun X, Kazama K, Yi B, et al. Ndrg1 signaling is essential for endothelial inflammation and vascular remodeling. Circ Res. 2023;132(3):306–19.

    Article  CAS  PubMed  Google Scholar 

  55. Ku DN. Blood flow in arteries. Annu Rev Fluid Mech. 1997;29(1):399–434.

    Article  Google Scholar 

  56. Molloy CP, Yao Y, Kammoun H, Bonnard T, Hoefer T, Alt K, et al. Shear-sensitive nanocapsule drug release for site-specific inhibition of occlusive thrombus formation. J Thromb Haemost : JTH. 2017;15(5):972–82.

  57. Torchilin VP, Papisov MI, Orekhova NM, Belyaev AA, Petrov AD, Ragimov SE. Magnetically driven thrombolytic preparation containing immobilized streptokinase-targeted transport and action. Haemostasis. 1988;18(2):113–6.

    CAS  PubMed  Google Scholar 

  58. Nguyen PD, O’Rear EA, Johnson AE, Patterson E, Whitsett TL, Bhakta R. Accelerated thrombolysis and reperfusion in a canine model of myocardial infarction by liposomal encapsulation of streptokinase. Circ Res. 1990;66(3):875–8.

    Article  CAS  PubMed  Google Scholar 

  59. Igor A, Tatyana V, Irina L, Katsiaryna D, Vladimir A. Efficiency of targeted delivery of streptokinase based on fibrin-specific liposomes in the in vivo experiment. Drug Deliv Transl Res. 2023;13(3):811–21.

    Article  CAS  PubMed  Google Scholar 

  60. Sun N, Ye Z, Hao T, Zheng S, Sun Y, Zhang Y, et al. Inhibition of arterial thrombus formation by blocking exposed collagen surface using lwwnsyy-poly(l-glutamic acid) nanoconjugate. Langmuir : The ACS Journal of Surfaces and Colloids. 2021;37(22):6792–9.

  61. Zhang X, Zhang Y, Wang Y, Wu J, Chen H, Zhao M, et al. Modifying ICCA with Trp-Phe-Phe to enhance in vivo activity and form nano-medicine. Int J Nanomed. 2020;15:465–81.

    Article  CAS  Google Scholar 

  62. Feng Q, Wang M, Muhtar E, Wang Y, Zhu H. Nanoparticles of a new small-molecule P-selectin inhibitor attenuate thrombosis, inflammation, and tumor growth in two animal models. Int J Nanomed. 2021;16:5777–95.

    Article  Google Scholar 

  63. Liu Y, Yang Z, Huang X, Yu G, Wang S, Zhou Z, et al. Glutathione-responsive self-assembled magnetic gold nanowreath for enhanced tumor imaging and imaging-guided photothermal therapy. ACS Nano. 2018;12(8):8129–37.

    Article  CAS  PubMed  Google Scholar 

  64. Ji W, Zhang Y, Deng Y, Li C, Kankala RK, Chen A. Nature-inspired nanocarriers for improving drug therapy of atherosclerosis. Regen Biomater. 2023;10:rbad069.

  65. Deng Q, Zhang L, Lv W, Liu X, Ren J, Qu X. Biological mediator-propelled nanosweeper for nonpharmaceutical thrombus therapy. ACS Nano. 2021;15(4):6604–13.

    Article  CAS  PubMed  Google Scholar 

  66. Sloand JN, Rokni E, Watson CT, Miller MA, Manning KB, Simon JC, et al. Ultrasound-responsive nanopeptisomes enable synchronous spatial imaging and inhibition of clot growth in deep vein thrombosis. Adv Healthcare Mater. 2021;10(16).

    Article  Google Scholar 

  67. Nan D, Jin H, Yang D, Yu W, Jia J, Yu Z, et al. Combination of polyethylene glycol-conjugated urokinase nanogels and urokinase for acute ischemic stroke therapeutic implications. Transl Stroke Res. 2021;12(5):844–57.

    Article  CAS  PubMed  Google Scholar 

  68. Cui W, Liu R, Jin H, Huang Y, Liu W, He M. The protective effect of polyethylene glycol-conjugated urokinase nanogels in rat models of ischemic stroke when administrated outside the usual time window. Biochem Biophys Res Commun. 2020;523(4):887–93.

    Article  CAS  PubMed  Google Scholar 

  69. Chavan YR, Tambe SM, Jain DD, Khairnar SV, Amin PD. Redefining the importance of polylactide-co-glycolide acid (PLGA) in drug delivery. Ann Pharm Fr. 2022;80(5):603–16.

    Article  CAS  PubMed  Google Scholar 

  70. Chen K, Wang Y, Liang H, Xia S, Liang W, Kong J, et al. Intrinsic biotaxi solution based on blood cell membrane cloaking enables fullerenol thrombolysis in vivo. ACS Appl Mater Interfaces. 2020;12(13):14958–70.

    Article  CAS  PubMed  Google Scholar 

  71. Wang Y, Zhang K, Qin X, Li T, Qiu J, Yin T, et al. Biomimetic nanotherapies: red blood cell based core-shell structured nanocomplexes for atherosclerosis management. Adv Sci (Weinheim, Baden-Wurttemberg, Germany). 2019;6(12):1900172.

  72. Huang Y, Gu B, Salles C, II, Taylor KA, Yu L, Ren J, et al. Fibrinogen-mimicking, multiarm nanovesicles for human thrombus-specific delivery of tissue plasminogen activator and targeted thrombolytic therapy. Sci Adv. 2021;7(23).

  73. Fang RH, Kroll AV, Gao W, Zhang L. Cell membrane coating nanotechnology. Adv Mater (Deerfield Beach, Fla). 2018;30(23).

  74. Huang M, Zhang SF, Lü S, Qi T, Yan J, Gao C, et al. Synthesis of mesoporous silica/polyglutamic acid peptide dendrimer with dual targeting and its application in dissolving thrombus. J Biomed Mater Res, Part A. 2019;107(8):1824–31.

    Article  CAS  Google Scholar 

  75. Marcano L, Orue I, Gandia D, Gandarias L, Weigand M, Abrudan RM, et al. Magnetic anisotropy of individual nanomagnets embedded in biological systems determined by axi-asymmetric x-ray transmission microscopy. ACS Nano. 2022;16(5):7398–408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lv J, Zhang L, Du W, Ling G, Zhang P. Functional gold nanoparticles for diagnosis, treatment and prevention of thrombus. J Controlled Release. 2022;345:572–85.

  77. Sha X, Dai Y, Song X, Liu S, Zhang S, Li J. The opportunities and challenges of silica nanomaterial for atherosclerosis. Int J Nanomed. 2021;16:701–14.

    Article  Google Scholar 

  78. Chen D, Zhu T, Fu W, Zhang H. Electrospun polycaprolactone/collagen nanofibers cross-linked with 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide/n-hydroxysuccinimide and genipin facilitate endothelial cell regeneration and may be a promising candidate for vascular scaffolds. Int J Nanomedicine. 2019;14:2127–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Chen JP, Yang PC, Ma YH, Lu YJ. Superparamagnetic iron oxide nanoparticles for delivery of tissue plasminogen activator. J Nanosci Nanotechnol. 2011;11(12):11089–94.

    Article  CAS  PubMed  Google Scholar 

  80. Xu J, Zhou Y, Nie H, Xiong Z, OuYang H, Huang L, et al. Hyperthermia-triggered uk release nanovectors for deep venous thrombosis therapy. J Mater Chem B. 2020;8(4):787–93.

  81. Liu S, Sun Y, Zhang T, Cao L, Zhong Z, Cheng H, et al. Upconversion nanoparticles regulated drug & gas dual-effective nanoplatform for the targeting cooperated therapy of thrombus and anticoagulation. Bioact Mater. 2022;18:91–103.

  82. Zhang Z, Chen Y, Zhang Y. Self-assembly of upconversion nanoparticles based materials and their emerging applications. Small. 2022;18(9).

    Article  PubMed  Google Scholar 

  83. Morya VK, Kim J, Kim EK. Algal fucoidan: Structural and size-dependent bioactivities and their perspectives. Appl Microbiol Biotechnol. 2012;93(1):71–82.

    Article  CAS  PubMed  Google Scholar 

  84. Falahati M, Sharifi M, Hagen T. Explaining chemical clues of metal organic framework-nanozyme nano-/micro-motors in targeted treatment of cancers: Benchmarks and challenges. J Nanobiotechnology. 2022;20(1):153.

  85. Zheng J, Qi R, Dai C, Li G, Sang M. Enzyme catalysis biomotor engineering of neutrophils for nanodrug delivery and cell-based thrombolytic therapy. ACS Nano. 2022;16(2):2330–44.

    Article  CAS  PubMed  Google Scholar 

  86. Nelson CE, Kintzing JR, Hanna A, Shannon JM, Gupta MK, Duvall CL. Balancing cationic and hydrophobic content of pegylated siRNA polyplexes enhances endosome escape, stability, blood circulation time, and bioactivity in vivo. ACS Nano. 2013;7(10):8870–80.

    Article  CAS  PubMed  Google Scholar 

  87. Ma B, Xu H, Wang Y, Yang L, Zhuang W, Li G, et al. Biomimetic-coated nanoplatform with lipid-specific imaging and ROS responsiveness for atherosclerosis-targeted theranostics. ACS Appl Mater Interfaces. 2021;13(30):35410–21.

    Article  CAS  PubMed  Google Scholar 

  88. Sun W, Xu Y, Yao Y, Yue J, Wu Z, Li H, et al. Self-oxygenation mesoporous MnO2 nanoparticles with ultra-high drug loading capacity for targeted arteriosclerosis therapy. J Nanobiotechnology. 2022;20(1):88.

  89. Xu C, Lei C, Yu C. Mesoporous silica nanoparticles for protein protection and delivery. Front Chem. 2019;7:290.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Zhang X, Liu J, Yang X, He G, Li B, Qin J, et al. CuCo2S4 nanocrystals as a nanoplatform for photothermal therapy of arterial inflammation. Nanoscale. 2019;11(19):9733–42.

  91. Li S, Zhang K, Ma Z, Zhang W, Song Z, Wang W, et al. Biomimetic nanoplatelets to target delivery hirudin for site-specific photothermal/photodynamic thrombolysis and preventing venous thrombus formation. Small. 2022;18(51):e2203184.

  92. Wu X, Liu K, Wang R, Yang G, Lin J, Liu X. Multifunctional CuBiS2 nanoparticles for computed tomography guided photothermal therapy in preventing arterial restenosis after endovascular treatment. Front Bioeng Biotech. 2020;8.

  93. Liu J, Wang P, Zhang X, Wang L, Wang D, Gu Z, et al. Rapid degradation and high renal clearance of Cu3BiS3 nanodots for efficient cancer diagnosis and photothermal therapy in vivo. ACS Nano. 2016;10(4):4587–98.

    Article  CAS  PubMed  Google Scholar 

  94. Fu D, Fang Q, Yuan F, Liu J, Ding H, Chen X, et al. Thrombolysis combined therapy using CuS@SiO2-PEG/uPA nanoparticles. Front Chem. 2021;9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Bhatia SN, Chen X, Dobrovolskaia MA, Lammers T. Cancer nanomedicine. Nat Rev Cancer. 2022;22(10):550–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Zhang H, Qu H, He Q, Gao L, Zhang H, Wang Y, et al. Thrombus-targeted nanoparticles for thrombin-triggered thrombolysis and local inflammatory microenvironment regulation. J Control Release. 2021;339:195–207.

  97. Zhang H, Pei Y, Gao L, He Q, Zhang H, Zhu L, et al. Shear force responsive and fixed-point separated system for targeted treatment of arterial thrombus. Nano Today. 2021;38.

    Article  CAS  Google Scholar 

  98. Guan Q, Dou H. Thrombus-targeting polymeric nanocarriers and their biomedical applications in thrombolytic therapy. Front Physiol. 2021;12.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Zhao Y, Xie R, Yodsanit N, Ye M, Wang Y, Gong S. Biomimetic fibrin-targeted and H2O2-responsive nanocarriers for thrombus therapy. Nano Today. 2020;35.

  100. Jung E, Noh J, Kang C, Yoo D, Song C, Lee D. Ultrasound imaging and on-demand therapy of peripheral arterial diseases using H2O2-activated bubble generating anti-inflammatory polymer particles. Biomaterials. 2018;179:175–85.

    Article  CAS  PubMed  Google Scholar 

  101. Kang C, Cho W, Park M, Kim J, Park S, Shin D, et al. H2O2-triggered bubble generating antioxidant polymeric nanoparticles as ischemia/reperfusion targeted nanotheranostics. Biomaterials. 2016;85:195–203.

    Article  CAS  PubMed  Google Scholar 

  102. Zhao Y, Xie R, Yodsanit N, Ye M, Wang Y, Wang B, et al. Hydrogen peroxide-responsive platelet membrane-coated nanoparticles for thrombus therapy. Biomaterials science. 2021;9(7):2696–708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Russell P, Hagemeyer CE, Esser L, Voelcker NH. Theranostic nanoparticles for the management of thrombosis. Theranostics. 2022;12(6):2773–800.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Ma Y, Ma Y, Gao M, Han Z, Jiang W, Gu Y, et al. Platelet-mimicking therapeutic system for noninvasive mitigation of the progression of atherosclerotic plaques. Adv Sci (Weinheim, Baden-Wurttemberg, Germany). 2021;8(8):2004128.

  105. Hu CM, Fang RH, Wang KC, Luk BT, Thamphiwatana S, Dehaini D, et al. Nanoparticle biointerfacing by platelet membrane cloaking. Nature. 2015;526(7571):118–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Mohale S, Kunde SS, Wairkar S. Biomimetic fabrication of nanotherapeutics by leukocyte membrane cloaking for targeted therapy. Colloids Surf, B. 2022;219.

    Article  CAS  Google Scholar 

  107. Wang Y, Zhang K, Li T, Maruf A, Qin X, Luo L, et al. Macrophage membrane functionalized biomimetic nanoparticles for targeted anti-atherosclerosis applications. Theranostics. 2021;11(1):164–80.

  108. Lee NH, You S, Taghizadeh A, Taghizadeh M, Kim HS. Cell membrane-cloaked nanotherapeutics for targeted drug delivery. Int J Mol Sci. 2022;23(4).

  109. Xu WJ, Cai JX, Li YJ, Wu JY, Xiang D. Recent progress of macrophage vesicle-based drug delivery systems. Drug Deliv Transl Res. 2022;12(10):2287–302.

    Article  PubMed  Google Scholar 

  110. Zhong Y, Gong WJ, Gao XH, Li YN, Liu K, Hu YG, et al. Synthesis and evaluation of a novel nanoparticle carrying urokinase used in targeted thrombolysis. J Biomed Mater Res, Part A. 2020;108(2):193–200.

    Article  CAS  Google Scholar 

  111. Luo X, Xie J, Zhou Z, Ma S, Wang L, Li M, et al. Virus-inspired gold nanorod-mesoporous silica core-shell nanoparticles integrated with TTF-EG3287 for synergetic tumor photothermal therapy and selective therapy for vascular thrombosis. ACS Appl Mater Interfaces. 2021;13(37):44013–27.

    Article  CAS  PubMed  Google Scholar 

  112. Zhong Y, Qin X, Wang Y, Qu K, Luo L, Zhang K, et al. "Plug and play" functionalized erythrocyte nanoplatform for target atherosclerosis management. ACS Appl Mater Interfaces. 2021;13(29):33862–73.

    Article  CAS  PubMed  Google Scholar 

  113. Thompson W, Papoutsakis ET. Similar but distinct: The impact of biomechanical forces and culture age on the production, cargo loading, and biological efficacy of human megakaryocytic extracellular vesicles for applications in cell and gene therapies. Bioeng Transl Med. 2023;8(5).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. De Matteis V, Rinaldi R. Toxicity assessment in the nanoparticle era. Adv Exp Med Biol. 2018;1048:1–19.

    Article  PubMed  Google Scholar 

  115. Wingard CJ, Walters DM, Cathey BL, Hilderbrand SC, Katwa P, Lin S, et al. Mast cells contribute to altered vascular reactivity and ischemia-reperfusion injury following cerium oxide nanoparticle instillation. Nanotoxicology. 2011;5(4):531–45.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (No. 21605161), Shenyang High-level Innovative Talent Program (RC180167), and Natural Science Foundation of Liaoning Province (2021-BS-105).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to conceptualizing and writing this manuscript.

Corresponding authors

Correspondence to Bo Hu or Ning Wang.

Ethics declarations

Ethics approval and consent to participate

No animal or human studies were performed to generate data for this article.

Consent for publication

All authors have reviewed this manuscript and approve of its publication.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shen, Y., Yu, Y., Zhang, X. et al. Progress of nanomaterials in the treatment of thrombus. Drug Deliv. and Transl. Res. 14, 1154–1172 (2024). https://doi.org/10.1007/s13346-023-01478-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13346-023-01478-6

Keywords

Navigation