Swarming magnetic nanorobots bio-interfaced by heparinoid-polymer brushes for in vivo safe synergistic thrombolysis

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Abstract

Biocompatible swarming magnetic nanorobots that work in blood vessels for safe and efficient targeted thrombolytic therapy in vivo are demonstrated. This is achieved by using magnetic beads elaborately grafted with heparinoid-polymer brushes (HPBs) upon the application of an alternating magnetic field B( t). Because of the dense surface charges bestowed by HPBs, the swarming nanorobots demonstrate reversible agglomeration-free reconfigurations, low hemolysis, anti-bioadhesion, and self-anticoagulation in high-ionic-strength blood environments. They are confirmed in vitro and in vivo to perform synergistic thrombolysis efficiently by “motile-targeting” drug delivery and mechanical destruction. Moreover, upon the completion of thrombolysis and removal of B( t), the nanorobots disassemble into dispersed particles in blood, allowing them to safely participate in circulation and be phagocytized by immune cells without apparent organ damage or inflammatory lesion. This work provides a rational multifaceted HPB biointerfacing design strategy for biomedical nanorobots and a general motile platform to deliver drugs for targeted therapies.

Abstract

Swarming magnetic nanorobots with heparinoid polymer brushes can perform safe and efficient thrombolysis in vivo.

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Most cited references 73

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Microorganisms such as bacteria and many eukaryotic cells propel themselves with hair-like structures known as flagella, which can exhibit a variety of structures and movement patterns. For example, bacterial flagella are helically shaped and driven at their bases by a reversible rotary engine, which rotates the attached flagellum to give a motion similar to that of a corkscrew. In contrast, eukaryotic cells use flagella that resemble elastic rods and exhibit a beating motion: internally generated stresses give rise to a series of bends that propagate towards the tip. In contrast to this variety of swimming strategies encountered in nature, a controlled swimming motion of artificial micrometre-sized structures has not yet been realized. Here we show that a linear chain of colloidal magnetic particles linked by DNA and attached to a red blood cell can act as a flexible artificial flagellum. The filament aligns with an external uniform magnetic field and is readily actuated by oscillating a transverse field. We find that the actuation induces a beating pattern that propels the structure, and that the external fields can be adjusted to control the velocity and the direction of motion.

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Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications.

Ajay Kumar Gupta, Mona Gupta (2005)

Superparamagnetic iron oxide nanoparticles (SPION) with appropriate surface chemistry have been widely used experimentally for numerous in vivo applications such as magnetic resonance imaging contrast enhancement, tissue repair, immunoassay, detoxification of biological fluids, hyperthermia, drug delivery and in cell separation, etc. All these biomedical and bioengineering applications require that these nanoparticles have high magnetization values and size smaller than 100 nm with overall narrow particle size distribution, so that the particles have uniform physical and chemical properties. In addition, these applications need special surface coating of the magnetic particles, which has to be not only non-toxic and biocompatible but also allow a targetable delivery with particle localization in a specific area. To this end, most work in this field has been done in improving the biocompatibility of the materials, but only a few scientific investigations and developments have been carried out in improving the quality of magnetic particles, their size distribution, their shape and surface in addition to characterizing them to get a protocol for the quality control of these particles. Nature of surface coatings and their subsequent geometric arrangement on the nanoparticles determine not only the overall size of the colloid but also play a significant role in biokinetics and biodistribution of nanoparticles in the body. The types of specific coating, or derivatization, for these nanoparticles depend on the end application and should be chosen by keeping a particular application in mind, whether it be aimed at inflammation response or anti-cancer agents. Magnetic nanoparticles can bind to drugs, proteins, enzymes, antibodies, or nucleotides and can be directed to an organ, tissue, or tumour using an external magnetic field or can be heated in alternating magnetic fields for use in hyperthermia. This review discusses the synthetic chemistry, fluid stabilization and surface modification of superparamagnetic iron oxide nanoparticles, as well as their use for above biomedical applications.

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Epidemiology of venous thromboembolism.

John Heit (2015)

Thrombosis can affect any venous circulation. Venous thromboembolism (VTE) includes deep-vein thrombosis of the leg or pelvis, and its complication, pulmonary embolism. VTE is a fairly common disease, particularly in older age, and is associated with reduced survival, substantial health-care costs, and a high rate of recurrence. VTE is a complex (multifactorial) disease, involving interactions between acquired or inherited predispositions to thrombosis and various risk factors. Major risk factors for incident VTE include hospitalization for surgery or acute illness, active cancer, neurological disease with leg paresis, nursing-home confinement, trauma or fracture, superficial vein thrombosis, and-in women-pregnancy and puerperium, oral contraception, and hormone therapy. Although independent risk factors for incident VTE and predictors of VTE recurrence have been identified, and effective primary and secondary prophylaxis is available, the occurrence of VTE seems to be fairly constant, or even increasing.

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Author and article information

Contributors

Manyi Yang:

ORCID: https://orcid.org/0000-0001-7342-7839

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Yaoyu Zhang:

ORCID: https://orcid.org/0009-0007-7980-1140

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: Validation

Fangzhi Mou:

ORCID: https://orcid.org/0000-0002-9644-8277

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing - original draftRole: Writing - review & editing

Chuan Cao: Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: Validation

Lingxia Yu: Role: InvestigationRole: MethodologyRole: ValidationRole: Writing - original draft

Zhi Li:

ORCID: https://orcid.org/0000-0002-9327-8110

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Jianguo Guan:

ORCID: https://orcid.org/0000-0002-2223-4524

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: 01 December 2023

Publication date (Electronic, pub): 29 November 2023

Volume: 9

Issue: 48

Electronic Location Identifier: eadk7251

Affiliations

[ ¹ ]State Key Laboratory of Advanced Technology for Materials Synthesis and Processing, International School of Materials Science and Engineering, Wuhan University of Technology, Wuhan 430070, P. R. China.

[ ² ]School of Medicine, Wuhan University of Science and Technology, Wuhan 430081, P. R. China.

[ ³ ]Department of Orthopedics, General Hospital of Chinese PLA Central Theater Command, Wuhan 430070, P. R. China.

[ ⁴ ]Wuhan Institute of Photochemistry and Technology, 7 North Bingang Road, Wuhan 430083, P. R. China.

Author notes

[* ]Corresponding author. Email: moufz@ 123456whut.edu.cn (F.M.); lizhi301@ 123456163.com (Z.L.); guanjg@ 123456whut.edu.cn (J.G.)

[†]

These authors contributed equally to this work.

Author information

Manyi Yang https://orcid.org/0000-0001-7342-7839

Yaoyu Zhang https://orcid.org/0009-0007-7980-1140

Fangzhi Mou https://orcid.org/0000-0002-9644-8277

Zhi Li https://orcid.org/0000-0002-9327-8110

Jianguo Guan https://orcid.org/0000-0002-2223-4524

Article

Publisher ID: adk7251

DOI: 10.1126/sciadv.adk7251

PMC ID: 10686566

PubMed ID: 38019908

SO-VID: c326ea47-9e6b-400f-a32d-fc0dc23c654b

Copyright © Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

History

Date received : 07 September 2023

Date accepted : 30 October 2023

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 52073222

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 21474078

Funded by: FundRef http://dx.doi.org/10.13039/501100003819, Natural Science Foundation of Hubei Province;

Award ID: 2019CFA048

Funded by: National Key Research and Development Project;

Award ID: 2021YFA1201400

Funded by: State Key Laboratory of Advanced Technology for Materials Synthesis and Processing (Wuhan University of Technology);

Award ID: 2023-KF-5

Funded by: Innovation Team in Key Areas of the Innovation Talent Promotion Plan of MOST of China;

Swarming magnetic nanorobots bio-interfaced by heparinoid-polymer brushes for in vivo safe synergistic thrombolysis

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Most cited references 73

Microscopic artificial swimmers.

Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications.

Epidemiology of venous thromboembolism.

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