Turning erythrocytes into functional micromotors

ACS Nano

Volumn 8, Issue 12, 2014, Pages 12041-12048

  Wu, Zhiguang ^a,b   Li, Tianlong ^a   Li, Jinxing ^a   Gao, Wei ^a   Xu, Tailin ^a   Christianson, Caleb ^a   Gao, Weiwei ^a   Galarnyk, Michael ^a   He, Qiang ^b   Zhang, Liangfang ^a   Wang, Joseph ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b HARBIN INSTITUTE OF TECHNOLOGY   (China)

Author keywords

biocompatibility; magnetic guidance; red blood cells; synthetic motor; ultrasound; whole blood

Indexed keywords

AIR NAVIGATION; BIOCOMPATIBILITY; BIOMECHANICS; CELLS; IRON OXIDES; MAGNETIC NANOPARTICLES; MAGNETISM; MEDICAL APPLICATIONS; MICROMOTORS; PROPULSION; ULTRASONICS;

ASYMMETRIC DISTRIBUTION; BIOMEDICAL APPLICATIONS; IRON OXIDE NANOPARTICLE; PROPULSION MECHANISMS; RED BLOOD CELL; STRUCTURAL FEATURE; SYNTHETIC MATERIALS; WHOLE BLOOD;

BLOOD;

ANIMAL; BIOMIMETICS; CELL LINE; CYTOLOGY; ERYTHROCYTE; MACROPHAGE; MALE; MICROTECHNOLOGY; MOUSE; PROCEDURES; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BIOMIMETICS; CELL LINE; ERYTHROCYTES; MACROPHAGES; MALE; MICE; MICROTECHNOLOGY;

EID: 84919742975     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn506200x     Document Type: Article

References (49)

1. Dreyfus, R.; Baudry, J.; Roper, M. L.; Fermigier, M.; Stone, H. A.; Bibette, J. Microscopic Artificial Swimmers Nature 2005, 437, 862-865
2. Paxton, W. F.; Kistler, K. C.; Olmeda, C. C.; Sen, A.; St. Angelo, S. K.; Cao, Y.; Mallouk, T. E.; Lammert, P. E.; Crespi, V. H. Catalytic Nanomotors: Autonomous Movement of Striped Nanorods J. Am. Chem. Soc. 2004, 126, 13424-13431
3. Wilson, D. A.; Nolte, R. J. M.; van Hest, J. C. M. Autonomous Movement of Platinum-Loaded Stomatocytes Nat. Chem. 2012, 4, 268-274
4. Weiss, P. S. Nanotechnology: A Molecular Four-Wheel Drive Nature 2011, 479, 187-188
5. Wang, J. Nanomachines: Fundamentals and Applications; Wiley-VCH: Weinheim, Germany, 2013.
6. Mei, Y. F.; Solovev, A. A.; Sanchez, S.; Schmidt, O. G. Rolled-up Nanotech on Polymers: From Basic Perception to Self-Propelled Catalytic Microengines Chem. Soc. Rev. 2011, 40, 2109-2119
7. Loget, G.; Kuhn, A. Electric Field-induced Chemical Locomotion of Conducting Objects Nat. Commun. 2011, 2, 535
8. van Rhee, P. G.; Rikken, R. S. M.; Abdelmohsen, L. K. E. A.; Maan, J. C.; Nolte, R. J. M.; van Hest, J. C. M.; Christianen, P. C. M.; Wilson, D. A. Polymersome Magneto-Valves for Reversible Capture and Release of Nanoparticles Nat. Commun. 2014, 5, 5010
9. Li, J.; Gao, W.; Dong, R.; Pei, A.; Sattayasamitsathit, S.; Wang, J. Nanomotor Lithography Nat. Commun. 2014, 5, 5026
10. Wu, J.; Balasubramanian, S.; Kagan, D.; Manesh, K. M.; Campuzano, S.; Wang, J. Motion-Based DNA Detection Using Catalytic Nanomotors Nat. Commun. 2010, 1, 36
11. Sengupta, S.; Patra, D.; Ortiz-Rivera, I.; Agrawal, A.; Shklyaev, S.; Dey, K. K.; Córdova-Figueroa, U.; Mallouk, T. E.; Sen, A. Self-Powered Enzyme Micropumps Nat. Chem. 2014, 6, 415-422
12. Ikezoe, Y.; Washino, G.; Uemura, T.; Kitagawa, S.; Matsui, H. Autonomous Motors of a Metal-Organic Framework Powered by Reorganization of Self-Assembled Peptides at Interfaces Nat. Mater. 2012, 11, 1081-1085
13. Solovev, A. A.; Sanchez, S.; Pumera, M.; Mei, Y. F.; Schmidt, O. G. Magnetic Control of Tubular Catalytic Microbots for the Transport, Assembly, and Delivery of Micro-objects Adv. Funct. Mater. 2010, 20, 2430-2435
14. Guix, M.; Mayorga-Martinez, C. C.; Merkoçi, A. Nano/Micromotors in (Bio)Chemical Science Applications Chem. Rev. 2014, 114, 6285-6322
15. Ismagilov, R. F.; Schwartz, A.; Bowden, N.; Whitesides, G. M. Autonomous Movement and Self-Assembly Angew. Chem., Int. Ed. 2002, 114, 652-654
16. Wang, W.; Duan, W.; Ahmed, S.; Mallouk, T. E.; Sen, A. Small Power: Autonomous Nano- and Micromotors Propelled by Self-Generated Gradients Nano Today 2013, 8, 531-554
17. Tottori, S.; Zhang, L.; Peyer, K. E.; Nelson, B. J. Assembly, Disassembly, and Anomalous Propulsion of Microscopic Helices Nano Lett. 2013, 13, 4263-4268
18. Wang, W.; Castro, L. A.; Hoyos, M.; Mallouk, T. E. Autonomous Motion of Metallic Microrods Propelled by Ultrasound ACS Nano 2012, 6, 6122-6132
19. Fischer, P.; Ghosh, A. Magnetically Actuated Propulsion at Low Reynolds Numbers: Towards Nanoscale Control Nanoscale 2011, 3, 557-563
20. Schamel, D.; Mark, A. G.; Gibbs, J. G.; Miksch, C.; Morozov, K. I.; Leshansky, A. M.; Fischer, P. Nanopropellers and Their Actuation in Complex Viscoelastic Media ACS Nano 2014, 8, 8794-8801
21. Zhang, L.; Hong, L.; Yu, Y.; Bae, S. C.; Granick, S. Nanoparticle-Assisted Surface Immobilization of Phospholipid Liposomes J. Am. Chem. Soc. 2006, 128, 9026-9027
22. Zhang, L.; Spurlin, T. A.; Gewirth, A. A.; Granick, S. Electrostatic Stitching in Gel-Phase Supported Phospholipid Bilayers J. Phys. Chem. B 2005, 110, 33-35
23. Love, K. T.; Mahon, K. P.; Levins, C. G.; Whitehead, K. A.; Querbes, W.; Dorkin, J. R.; Qin, J.; Cantley, W.; Qin, L. L.; Racie, T. et al. Lipid-like Materials for Low-Dose, In Vivo Gene Silencing Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 1864-1869
24. Celiz, A. D.; Smith, J. G. W.; Langer, R.; Anderson, D. G.; Winkler, D. A.; Barrett, D. A.; Davies, M. C.; Young, L. E.; Denning, C.; Alexander, M. R. Materials for Stem Cell Factories of the Future Nat. Mater. 2014, 13, 570-579
25. Yang, F.; Cho, S. W.; Son, S. M.; Bogatyrev, S. R.; Singh, D.; Green, J. J.; Mei, Y.; Park, S.; Bhang, S. H.; Kim, B. S. et al. Genetic Engineering of Human Stem Cells for Enhanced Angiogenesis Using Biodegradable Polymeric Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 3317-3322
26. Hu, C. M.; Fang, R. H.; Luk, B. T.; Zhang, L. Nanoparticle-Detained Toxins for Safe and Effective Vaccination Nat. Nanotechnol. 2013, 8, 933-938
27. Zhang, K.; Zhang, L.; Weinreb, R. N. Ophthalmic Drug Discovery: Novel Targets and Mechanisms for Retinal Diseases and Glaucoma Nat. Rev. Drug Discovery 2012, 11, 541-559
28. Pierigè, F.; Serafini, S.; Rossi, L.; Magnani, M. Cell-Based Drug Delivery Adv. Drug Delivery Rev. 2008, 60, 286-295
29. Brähler, M.; Georgieva, R.; Buske, N.; Müller, A.; Müller, S.; Pinkernelle, J.; Teichgräber, U.; Voigt, A.; Bäumler, H. Magnetite-Loaded Carrier Erythrocytes as Contrast Agents for Magnetic Resonance Imaging Nano Lett. 2006, 6, 2505-2509
30. Lee, J.; Choi, J.; Park, J. H.; Kim, M. H.; Hong, D.; Cho, H.; Yang, S. H.; Choi, I. S. Cytoprotective Silica Coating of Individual Mammalian Cells through Bioinspired Silicification Angew. Chem., Int. Ed. 2014, 53, 8056-8059
31. Muzykantov, V. R. Drug Delivery by Red Blood Cells: Vascular Carriers Designed by Mother Nature Expert Opin. Drug Delivery 2010, 7, 403-427
32. Yoo, J. W.; Irvine, D. J.; Discher, D. E.; Mitragotri, S. Bio-Inspired, Bioengineered and Biomimetic Drug Delivery Carriers Nat. Rev. Drug Discovery 2011, 10, 521-535
33. Ding, X.; Lin, S.-C. S.; Kiraly, B.; Yue, H.; Li, S.; Chiang, I. K.; Shi, J.; Benkovic, S. J.; Huang, T. J. On-Chip Manipulation of Single Microparticles, Cells, and Organisms Using Surface Acoustic Waves Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 11105-11109
34. Wang, W.; Li, S.; Mair, L.; Ahmed, S.; Huang, T. J.; Mallouk, T. E. Acoustic Propulsion of Nanorod Motors Inside Living Cells Angew. Chem., Int. Ed 2014, 126, 3265-3268
35. Nadal, F.; Lauga, E. Asymmetric Steady Streaming as a Mechanism for Acoustic Propulsion of Rigid Bodies Phys. Fluids 2014, 26, 082001
36. Venugopalan, P. L.; Sai, R.; Chandorkar, Y.; Basu, B.; Shivashankar, S.; Ghosh, A. Conformal Cytocompatible Ferrite Coatings Facilitate the Realization of a Nanovoyager in Human Blood Nano Lett. 2014, 14, 1968-1975
37. Kolesnikova, T. A.; Skirtach, A. G.; Möhwald, H. Red Blood Cells and Polyelectrolyte Multilayer Capsules: Natural Carriers versus Polymer-Based Drug Delivery Vehicles Expert Opin. Drug Delivery 2013, 10, 47-58
38. Delcea, M.; Sternberg, N.; Yashchenok, A. M.; Georgieva, R.; Bäumler, H.; Möhwald, H.; Skirtach, A. G. Nanoplasmonics for Dual-Molecule Release through Nanopores in the Membrane of Red Blood Cells ACS Nano 2012, 6, 4169-4180
39. Zhang, E.; Kircher, M. F.; Koch, M.; Eliasson, L.; Goldberg, S. N.; Renström, E. Dynamic Magnetic Fields Remote-Control Apoptosis via Nanoparticle Rotation ACS Nano 2014, 8, 3192-3201
40. Valberg, P. A.; Feldman, H. A. Magnetic Particle Motions within Living Cells. Measurement of Cytoplasmic Viscosity and Motile Activity Biophys. J. 1987, 52, 551-561
41. Wilhelm, C.; Billotey, C.; Roger, J.; Pons, J. N.; Bacri, J. C.; Gazeau, F. Intracellular Uptake of Anionic Superparamagnetic Nanoparticles as a Function of Their Surface Coating Biomaterials 2003, 24, 1001-1011
42. Gao, W.; Sattayasamitsathit, S.; Orozco, J.; Wang, J. Efficient Bubble Propulsion of Polymer-Based Microengines in Real-Life Environments Nanoscale 2013, 5, 8909-8914
43. Hu, C. M. J.; Zhang, L.; Aryal, S.; Cheung, C.; Fang, R. H.; Zhang, L. Erythrocyte Membrane-Camouflaged Polymeric Nanoparticles as a Biomimetic Delivery Platform Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 10980-10985
44. Hu, C. M. J.; Fang, R. H.; Zhang, L. Erythrocyte-Inspired Delivery Systems Adv. Healthcare Mater. 2012, 1, 537-547
45. Fang, R. H.; Hu, C.M. J.; Zhang, L. Nanoparticles Disguised as Red Blood Cells To Evade the Immune System Expert Opin. Biol. Ther. 2012, 12, 385-389
46. Wang, C.; Sun, X.; Cheng, L.; Yin, S.; Yang, G.; Li, Y.; Liu, Z. Multifunctional Theranostic Red Blood Cells for Magnetic-Field-Enhanced In Vivo Combination Therapy of Cancer Adv. Mater. 2014, 26, 4794-4802
47. Lee, D.; Cohen, R. E.; Rubner, M. F. Heterostructured Magnetic Nanotubes Langmuir 2006, 23, 123-129
48. Xu, T.; Soto, F.; Gao, W.; Garcia-Gradilla, V.; Li, J.; Zhang, X.; Wang, J. Ultrasound-Modulated Bubble Propulsion of Chemically Powered Microengines J. Am. Chem. Soc. 2014, 136, 8552-8555
49. Garcia-Gradilla, V.; Orozco, J.; Sattayasamitsathit, S.; Soto, F.; Kuralay, F.; Pourazary, A.; Katzenberg, A.; Gao, W.; Shen, Y.; Wang, J. Functionalized Ultrasound-Propelled Magnetically Guided Nanomotors: Toward Practical Biomedical Applications ACS Nano 2013, 7, 9232-9240