Single-particle tracking for studying nanomaterial dynamics: Applications and fundamentals in drug delivery

Nanomedicine

Volumn 9, Issue 6, 2014, Pages 913-927

  Zagato, Elisa ^a   Forier, Katrien ^a   Martens, Thomas ^a   Neyts, Kristiaan ^a   Demeester, Jo ^a   Smedt, Stefaan De ^a   Remaut, Katrien ^a   Braeckmans, Kevin ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

diffusion; drug delivery; fluorescence microscopy; nanoparticles; single particle tracking; transport

Indexed keywords

COLLAGEN; HYALURONIC ACID; MACROGOL; NANOCARRIER; NANOMATERIAL; POLYSTYRENE; DRUG CARRIER; NANOPARTICLE;

ANALYTIC METHOD; CELL COMPARTMENTALIZATION; DRUG ADMINISTRATION ROUTE; DRUG DELIVERY SYSTEM; DYNAMICS; ENDOSOME; HUMAN; MACROMOLECULE; MICROSCOPY; NANOMEDICINE; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; REVIEW; SINGLE PARTICLE TRACKING; TARGET CELL; ANIMAL; FLUORESCENCE MICROSCOPY; PROCEDURES; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HUMANS; MICROSCOPY, FLUORESCENCE; NANOPARTICLES;

EID: 84903762820     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.14.43     Document Type: Review

References (89)

1. Remaut K, Sanders NN, De Geest BG, Braeckmans K, Demeester J, De Smedt SC. Nucleic acid delivery: where material sciences and bio-sciences meet. Mat. Sci. Eng. R 58(3-5), 117-161 (2007).
2. Konstan MW, Davis PB, Wagener JS et al. Compacted DNA nanoparticles administered to the nasal mucosa of cystic fibrosis subjects are safe and demonstrate partial to complete cystic fibrosis transmembrane regulator reconstitution. Hum. Gene Ther. 15(12), 1255-1269 (2004). (Pubitemid 40052437)
3. Farjo R, Skaggs J, Quiambao AB, Cooper MJ, Naash MI. Efficient non-viral ocular gene transfer with compacted DNA nanoparticles. PLoS ONE 1, e38 (2006).
4. Lechardeur D, Sohn KJ, Haardt M et al. Metabolic instability of plasmid DNA in the cytosol: a potential barrier to gene transfer. Gene Ther. 6(4), 482-497 (1999). (Pubitemid 29192657)
5. Vercauteren D, Rejman J, Martens TF, Demeester J, De Smedt SC, Braeckmans K. On the cellular processing of non-viral nanomedicines for nucleic acid delivery: mechanisms and methods. J. Control. Release 161(2), 566-581 (2012).
6. Braeckmans K, Buyens K, Naeye B et al. Advanced fluorescence microscopy methods illuminate the transfection pathway of nucleic acid nanoparticles. J. Control. Release 148(1), 69-74 (2010).
7. Ruthardt N, Lamb DC, Brauchle C. Single-particle tracking as a quantitative microscopy-based approach to unravel cell entry mechanisms of viruses and pharmaceutical nanoparticles. Mol. Ther. 19(7), 1199-1211 (2011).
8. Huang F, Dempsey C, Chona D, Suh J. Quantitative nanoparticle tracking: applications to nanomedicine. Nanomedicine 6(4), 693-700 (2011).
9. Xu Q, Boylan NJ, Suk JS et al. Nanoparticle diffusion in, and microrheology of, the bovine vitreous ex vivo. J. Control. Release 167(1), 76-84 (2013).
10. Lai SK, Wang YY, Hida K, Cone R, Hanes J. Nanoparticles reveal that human cervicovaginal mucus is riddled with pores larger than viruses. Proc. Natl Acad. Sci. USA 107(2), 598-603 (2010).
11. Nance EA, Woodworth GF, Sailor KA et al. A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Sci. Transl. Med. 4(149), 149ra119 (2012).
12. Forier K, Messiaen AS, Raemdonck K et al. Transport of nanoparticles in cystic fibrosis sputum and bacterial biofilms by single-particle tracking microscopy. Nanomedicine 8(6), 935-949 (2013).
13. Lai SK, Ohanlon DE, Harrold S et al. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus. Proc. Natl Acad. Sci. USA 104(5), 1482-1487 (2007). (Pubitemid 46214616)
14. Braeckmans K, Buyens K, Bouquet W et al. Sizing nanomatter in biological fluids by fluorescence single particle tracking. Nano Lett. 10(11), 4435-4442 (2010).
15. Martens TF, Vercauteren D, Forier K et al. Measuring the intravitreal mobility of nanomedicines with single-particle tracking microscopy. Nanomedicine 8(12), 1955-1968 (2013).
16. Vercauteren D, Deschout H, Remaut K et al. Dynamic colocalization microscopy to characterize intracellular trafficking of nanomedicines. ACS Nano 5(10), 7874-7884 (2011).
17. Deschout H, Martens T, Vercauteren D et al. Correlation of dual colour single particle trajectories for improved detection and analysis of interactions in living cells. Int. J. Mol. Sci. 14(8), 16485-16514 (2013).
18. Dupont A, Stirnnagel K, Lindemann D, Lamb DC. Tracking image correlation: combining single-particle tracking and image correlation. Biophys. J. 104(11), 2373-2382 (2013).
19. Bausinger R, Von Gersdorff K, Braeckmans K et al. The transport of nanosized gene carriers unraveled by live-cell imaging. Angew. Chem. 45(10), 1568-1572 (2006). (Pubitemid 44105272)
20. De Bruin K, Ruthardt N, Von Gersdorff K et al. Cellular dynamics of EGF receptor-targeted synthetic viruses. Mol. Ther. 15(7), 1297-1305 (2007). (Pubitemid 46965326)
21. Sahay G, Querbes W, Alabi C et al. Efficiency of siRNA delivery by lipid nanoparticles is limited by endocytic recycling. Nat. Biotechnol. 31(7), 653-658 (2013).
22. Naeye B, Deschout H, Roding M et al. Hemocompatibility of siRNA loaded dextran nanogels. Biomaterials 32(34), 9120-9127 (2011).
23. Filipe V, Poole R, Kutscher M, Forier K, Braeckmans K, Jiskoot W. Fluorescence single particle tracking for the characterization of submicron protein aggregates in biological fluids and complex formulations. Pharm. Res. 28(5), 1112-1120 (2011).
24. Wang YY, Lai SK, Suk JS, Pace A, Cone R, Hanes J. Addressing the PEG mucoadhesivity paradox to engineer nanoparticles that slip through the human mucus barrier. Angew. Chem. Int. Ed. Engl. 47(50), 9726-9729 (2008).
25. Suk JS, Lai SK, Wang YY et al. The penetration of fresh undiluted sputum expectorated by cystic fibrosis patients by non-adhesive polymer nanoparticles. Biomaterials 30(13), 2591-2597 (2009).
26. Suh J, Dawson M, Hanes J. Real-time multiple-particle tracking: applications to drug and gene delivery. Adv. Drug Deliv. Rev. 57(1), 63-78 (2005). (Pubitemid 39424064)
27. Hallaj-Nezhadi S, Dass CR, Lotfipour F. Intraperitoneal delivery of nanoparticles for cancer gene therapy. Future Oncol. 9(1), 59-68 (2012).
28. Guarnieri D, Guaccio A, Fusco S, Netti P. Effect of serum proteins on polystyrene nanoparticle uptake and intracellular trafficking in endothelial cells. J. Nanopart. Res. 13(9), 4295-4309 (2011).
29. Salvati A, Pitek AS, Monopoli MP et al. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol. 8(2), 137-143 (2013).
30. Roding M, Deschout H, Braeckmans K, Rudemo M. Measuring absolute number concentrations of nanoparticles using single-particle tracking. Phys. Rev. E Stat. Nonlin. Soft Matter. Phys. 84(3 Pt 1), 031920 (2011).
31. Roding M, Deschout H, Braeckmans K, Rudemo M. Measuring absolute nanoparticle number concentrations from particle count time series. J. Microscopy 251(1), 19-26 (2013).
32. Roding M, Deschout H, Braeckmans K, Sarkka A, Rudemo M. Self-calibrated concentration measurements of polydisperse nanoparticles. J. Microscopy 252(1), 79-88 (2013).
33. Filipe V, Poole R, Oladunjoye O, Braeckmans K, Jiskoot W. Detection and characterization of subvisible aggregates of monoclonal IgG in serum. Pharm. Res. 29(8), 2202-2212 (2012).
34. Wohlfart S, Gelperina S, Kreuter J. Transport of drugs across the blood-brain barrier by nanoparticles. J. Control. Release 161(2), 264-273 (2012).
35. Thorne RG, Nicholson C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc. Natl Acad. Sci. USA 103(14), 5567-5572 (2006).
36. Roy I, Vij N. Nanodelivery in airway diseases: challenges and therapeutic applications. Nanomedicine 6(2), 237-244 (2010).
37. Georgiades P, Pudney PD, Thornton DJ, Waigh T. Particle tracking microrheology of purified gastrointestinal mucins. Biopolymers 101(4), 366-377 (2014).
38. Cone RA. Barrier properties of mucus. Adv. Drug Deliv. Rev. 61(2), 75-85 (2009).
39. Ensign LM, Schneider C, Suk JS, Cone R, Hanes J. Mucus penetrating nanoparticles: biophysical tool and method of drug and gene delivery. Ad. Mater. 24(28), 3887-3894 (2012).
40. Lai SK, Wang YY, Hanes J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. Adv. Drug Deliv. Rev. 61(2), 158-171 (2009).
41. Ensign LM, Cone R, Hanes J. Oral drug delivery with polymeric nanoparticles: the gastrointestinal mucus barriers. Adv. Drug Deliv. Rev. 64(6), 557-570 (2012).
42. Amsden B. An Obstruction-Scaling Model for Diffusion in Homogeneous Hydrogels. Macromolecules 32(3), 874-879 (1999).
43. Naik R, Mukhopadhyay A, Ganguli M. Gene delivery to the retina: focus on non-viral approaches. Drug Discov. Today 14(5-6), 306-315 (2009).
44. Koo H, Moon H, Han H et al. The movement of self-assembled amphiphilic polymeric nanoparticles in the vitreous and retina after intravitreal injection. Biomaterials 33(12), 3485-3493 (2012).
45. Peeters L, Sanders NN, Braeckmans K et al. Vitreous: a barrier to nonviral ocular gene therapy. Invest. Ophthal. Vis. Sci. 46(10), 3553-3561 (2005). (Pubitemid 44264656)
46. Rejman J, Oberle V, Zuhorn IS, Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin-and caveolae-mediated endocytosis. Biochem. J. 377(Pt 1), 159-169 (2004). (Pubitemid 38114443)
47. Adler AF, Leong KW. Emerging links between surface nanotechnology and endocytosis: impact on nonviral gene delivery. Nano Today 5(6), 553-569 (2010).
48. Dobay MP, Schmidt A, Mendoza E, Bein T, Radler JO. Cell type determines the light-induced endosomal escape kinetics of multifunctional mesoporous silica nanoparticles. Nano Lett. 13(3), 1047-1052 (2013).
49. Kim JA, Aberg C, Salvati A, Dawson KA. Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. Nat. Nanotechnol. 7(1), 62-68 (2012).
50. Iversen TG, Skotland T, Sandvig K. Endocytosis and intracellular transport of nanoparticles: Present knowledge and need for future studies. Nano Today 6(2), 176-185 (2011).
51. Hofmann D, Mailander V. Pharmacology of nanocarriers on the microscale: importance of uptake mechanisms and intracellular trafficking for efficient drug delivery. Nanomedicine 8(3), 321-323 (2013).
52. Nguyen J, Szoka FC. Nucleic Acid Delivery: The Missing Pieces of the Puzzle? Acc. Chem. Res.45(7), 1153-1162 (2012).
53. Suh J, Choy KL, Lai SK et al. PEGylation of nanoparticles improves their cytoplasmic transport. Int. J. Nanomedicine 2(4), 735-741 (2007).
54. Kim AJ, Boylan NJ, Suk JS, Lai SK, Hanes J. Non-degradative intracellular trafficking of highly compacted polymeric DNA nanoparticles. J. Control. Release 158(1), 102-107 (2012).
55. Lai SK, Hida K, Man ST et al. Privileged delivery of polymer nanoparticles to the perinuclear region of live cells via a non-clathrin, non-degradative pathway. Biomaterials 28(18), 2876-2884 (2007). (Pubitemid 46482662)
56. Lai SK, Hida K, Chen C, Hanes J. Characterization of the intracellular dynamics of a non-degradative pathway accessed by polymer nanoparticles. J. Control. Release 125(2), 107-111 (2008). (Pubitemid 350299609)
57. Rehman Z, Zuhorn IS, Hoekstra D. How cationic lipids transfer nucleic acids into cells and across cellular membranes: recent advances. J. Control. Release 166(1), 46-56 (2013).
58. Sandin P, Fitzpatrick LW, Simpson JC, Dawson KA. High-speed imaging of Rab family small GTPases reveals rare events in nanoparticle trafficking in living cells. ACS Nano 6(2), 1513-1521 (2012).
59. Suh J, An Y, Tang BC, Dempsey C, Huang F, Hanes J. Real-time gene delivery vector tracking in the endo-lysosomal pathway of live cells. Microscopy Res. Tech. 75(5), 691-697 (2012).
60. Lakadamyali M, Rust MJ, Babcock HP, Zhuang X. Visualizing infection of individual influenza viruses. Proc. Natl Acad. Sci. USA 100(16), 9280-9285 (2003). (Pubitemid 37033920)
61. Cheezum MK, Walker WF, Guilford WH. Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys. J. 81(4), 2378-2388 (2001). (Pubitemid 32917184)
62. Bachir AI, Durisic N, Hebert B, Grutter P, Wiseman PW. Characterization of blinking dynamics in quantum dot ensembles using image correlation spectroscopy. J. Appl. Phys. 99(6), 064503 (2006).
63. Deschout H, Neyts K, Braeckmans K. The influence of movement on the localization precision of sub-resolution particles in fluorescence microscopy. J. Biophotonics 5(1), 97-109 (2012).
64. Li W, Liu R, Wang Y, Zhao Y, Gao X. Temporal techniques: dynamic tracking of nanomaterials in live cells. Small 9(9-10), 1585-1594 (2013).
65. Zhou X, Wang L. Uses of single-particle tracking in living cells. Drug Discov. Ther. 4(2), 62-69 (2010).
66. Chang JC, Rosenthal SJ. Real-time quantum dot tracking of single proteins. Methods Mol. Biol. 726, 51-62 (2011).
67. Delehanty JB, Mattoussi H, Medintz IL. Delivering quantum dots into cells: strategies, progress and remaining issues. Anal. Bioanal. Chem. 393(4), 1091-1105 (2009).
68. Strano MS, Jin H. Where is it heading? Single-particle tracking of single-walled carbon nanotubes. ACS Nano 2(9), 1749-1752 (2008).
69. Fu C-C, Lee H-Y, Chen K et al. Characterization and application of single fluorescent nanodiamonds as cellular biomarkers. Proc. Natl Acad. Sci. USA 104(3), 727-732 (2007). (Pubitemid 46154678)
70. He X, Gao J, Gambhir SS, Cheng Z. Near-infrared fluorescent nanoprobes for cancer molecular imaging: status and challenges. Trends Mol. Med. 16(12), 574-583 (2010).
71. Brandenburg B, Zhuang X. Virus trafficking - learning from single-virus tracking. Nat. Rev. Microbiol. 5(3), 197-208 (2007). (Pubitemid 46291279)
72. Ritter JG, Veith R, Siebrasse JP, Kubitscheck U. High-contrast single-particle tracking by selective focal plane illumination microscopy. Optics Express 16(10), 7142-7152 (2008). (Pubitemid 351697398)
73. Ritter JG, Veith R, Veenendaal A, Siebrasse JP, Kubitscheck U. Light sheet microscopy for single molecule tracking in living tissue. PLoS ONE 5(7), e11639 (2010).
74. Spille JH, Kaminski T, Konigshoven HP, Kubitscheck U. Dynamic three-dimensional tracking of single fluorescent nanoparticles deep inside living tissue. Optics Express 20(18), 19697-19707 (2012).
75. Schiffmann DA, Dikovskaya D, Appleton PL et al. Open microscopy environment and findspots: integrating image informatics with quantitative multidimensional image analysis. Biotechniques 41(2), 199-208 (2006). (Pubitemid 46542604)
76. Jaqaman K, Loerke D, Mettlen M et al. Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5(8), 695-702 (2008).
77. Sutherland W. LXXV. A dynamical theory of diffusion for non-electrolytes and the molecular mass of albumin. Philosophical Magazine Series 6 9(54), 781-785 (1905).
78. Metzler R, Klafter J. The random walks guide to anomalous diffusion: a fractional dynamics approach. Phys. Rep. 339(1), 1-77 (2000).
79. Katayama Y, Burkacky O, Meyer M, Brauchle C, Gratton E, Lamb DC. Real-time nanomicroscopy via three-dimensional single-particle tracking. Chemphyschem 10(14), 2458-2464 (2009).
80. Levi V, Ruan Q, Gratton E. 3-D particle tracking in a two-photon microscope: application to the study of molecular dynamics in cells. Biophys. J. 88(4), 2919-2928 (2005). (Pubitemid 40976156)
81. Toprak E, Balci H, Blehm BH, Selvin PR. Three-dimensional particle tracking via bifocal imaging. Nano Lett. 7(7), 2043-2045 (2007). (Pubitemid 47197589)
82. Prabhat P, Gan Z, Chao J et al. Elucidation of intracellular recycling pathways leading to exocytosis of the Fc receptor, FcRn, by using multifocal plane microscopy. Proc. Natl Acad. Sci. USA 104(14), 5889-5894 (2007). (Pubitemid 47175629)
83. Ram S, Prabhat P, Chao J, Ward ES, Ober RJ. High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells. Biophys. J. 95(12), 6025-6043 (2008).
84. Huang B, Wang W, Bates M, Zhuang X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319(5864), 810-813 (2008). (Pubitemid 351225870)
85. Thompson MA, Lew MD, Badieirostami M, Moerner WE. Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function. Nano Lett. 10(1), 211-218 (2010).
86. Lee SH, Roichman Y, Yi GR et al. Characterizing and tracking single colloidal particles with video holographic microscopy. Optics express 15(26), 18275-18282 (2007).
87. Warnasooriya N, Joud F, Bun P et al. Imaging gold nanoparticles in living cell environments using heterodyne digital holographic microscopy. Optics express 18(4), 3264-3273 (2010).
88. Uphoff S, Reyes-Lamothe R, Garza De Leon F, Sherratt DJ, Kapanidis AN. Single-molecule DNA repair in live bacteria. Proc. Natl Acad. Sci. USA 110(20), 8063-8068 (2013).
89. Deschout H, Raemdonck K, Stremersch S et al. On-chip light sheet illumination enables diagnostic size and concentration measurements of membrane vesicles in biofluids. Nanoscale 6(3), 1741-1747 (2013).