Recombinant protein-stabilized monodisperse microbubbles with tunable size using a valve-based microfluidic device

Langmuir

Volumn 30, Issue 42, 2014, Pages 12610-12618

  Angilè, Francesco E ^a   Vargo, Kevin B ^a   Sehgal, Chandra M ^b   Hammer, Daniel A ^a   Lee, Daeyeon ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRO-FLUIDIC DEVICES; MICROBUBBLES; MONO-DISPERSE; TUNABLE SIZES;

RECOMBINANT PROTEIN; VEGETABLE PROTEIN;

CHEMISTRY; MICROBUBBLE; MICROFLUIDIC ANALYSIS; PARTICLE SIZE; PROCEDURES;

MICROBUBBLES; MICROFLUIDIC ANALYTICAL TECHNIQUES; PARTICLE SIZE; PLANT PROTEINS; RECOMBINANT PROTEINS;

EID: 84908341794     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la502610c     Document Type: Article

References (63)

1. Kiessling, F.; Fokong, S.; Koczera, P.; Lederle, W.; Lammers, T. Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics J. Nucl. Med. 2012, 53, 345-348
2. de Jong, N.; Cate, F. T.; Lancée, C.; Roelandt, J.; Bom, N. Principles and recent developments in ultrasound contrast agents Ultrasonics 1991, 29, 324-330
3. Del Vecchio, S.; Zannetti, A.; Fonti, R. Nuclear Imaging in cancer theranostic Q. J. Nucl. Med. Mol. Imaging 2007, 51, 152-163
4. Segers, T.; Versluis, M. Acoustic bubble sorting for ultrasound contrast agent enrichment Lab Chip 2014, 14, 1705-1714
5. Talu, E.; Hettiarachchi, K.; Zhao, S.; Powell, R. L.; Lee, A. P.; Longo, L.; Dayton, P. A. Tailoring the size distribution of ultrasound contrast agents: possible method for improving sensitivity in molecular imaging Mol. Imaging 2007, 6, 384-392
6. Streeter, J. E.; Gessner, R.; Iman Miles, I.; Dayton, P. A. Improving sensitivity in ultrasound molecular imaging by tailoring contrast agent size distribution: in vivo studies Mol. Imaging 2010, 9, 87-95
7. Kaya, M.; Feingold, S.; Hettiarachchi, K.; Lee, A. P.; Dayton, P. A. Acoustic responses of monodisperse lipid-encapsulated microbubble contrast agents produced by flow focusing Bubble Sci. Eng. Technol. 2010, 2, 33-40
8. Feshitan, J. A.; Chen, C. C.; Kwan, J. J.; Borden, M. A. Microbubble size isolation by differential centrifugation J. Colloid Interface Sci. 2009, 329, 316-324
9. Wood, A. K.; Ansaloni, S.; Ziemer, L. S.; Lee, W. M.-F.; Feldman, C. M.; Sehgal, M. D. The antivascular action of physiotherapy ultrasound on murine tumors Ultrasound Med. Biol. 2005, 31, 1403-1410
10. Wood, A. K.; Bunte, R. M.; Cohen, J. D.; Tsai, J. H.; Lee, W. M.-F.; Sehgal, C. M. The antivascular action of physiotherapy ultrasound on a murine tumor: role of a microbubble contrast agent Ultrasound Med. Biol. 2007, 33, 1901-1910
11. Wood, A. K.; Bunte, R. M.; Price, H. E.; Deitz, M. S.; Tsai, J. H.; Lee, W. M.-F.; Sehgal, C. M. The disruption of murine tumor neovasculature by low-intensity ultrasounds comparison between 1- and 3-MHz sonication frequencies Acad. Radiol. 2008, 15, 1133-1141
12. Wood, A. K.; Bunte, R. M. Acute increases in murine tumor echogenicity after antivascular ultrasound therapy a pilot preclinical study J. Ultrasound. Med. 2009, 28 (6) 795-800
13. Wood, A. K.; Schultz, S. M.; Lee, W. M.-F.; Bunte, R. M.; Sehgal, C. M. Antivascular ultrasound therapy extends survival of mice with implanted melanomas Ultrasound Med. Biol. 2010, 36, 853-857
14. Goertz, D.; Karshafian, R.; Hynynen, K. Antivascular effects of pulsed low intensity ultrasound and microbubbles in mouse tumors IEEE Int. Ultrason. Symp. 2008, 670-673
15. Chin, C. T.; Raju, B.; Shevchenko, T.; Klibanov, A. Control and reversal of tumor growth by ultrasound activated microbubbles IEEE Int. Ultrason. Symp. 2009, 77-80
16. Gañán Calvo, A. M. Perfectly monodisperse microbubbling by capillary flow focusing: An alternate physical description and universal scaling Phys. Rev. E 2004, 69, 027301
17. Anna, S. L.; Bontoux, N.; Stone, H. A. Formation of dispersions using "flow focusing" in microchannels Appl. Phys. Lett. 2003, 82, 364-366
18. Garstecki, P.; Stone, H. A.; Whitesides, G. M. Mechanism for flow-rate controlled breakup in confined geometries: a route to monodisperse emulsions Phys. Rev. Lett. 2005, 94, 164501
19. Dollet, B.; van Hoeve, W.; Raven, J.-P.; Marmottant, P.; Versluis, M. Role of the channel geometry on the bubble pinch-off in flow-focusing devices Phys. Rev. Lett. 2008, 100, 034504
20. Park, J. I.; Tumarkin, E.; Kumacheva, E. Microbubbles loaded with nanoparticles: a route to multiple imaging modalities Macromol. Rapid Commun. 2010, 31, 222-227
21. Huang, A. H. C. Oil bodies and oleosins in seeds Annu. Rev. Plant Physiol. Plant Mol. Biol. 1992, 43, 177-200
22. Vargo, K. B.; Parthasarathy, R.; Hammer, D. A. Self-assembly of tunable protein suprastructures from recombinant oleosin Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 11657-11662
23. Suslick, K. S.; Grinstaff, M. W. Nonaqueous liquid filled microcapsules Polym. Prepr. 1991, 32, 255-256
24. Cavalieri, F.; Ashokkumar, M.; Grieser, F.; Caruso, F. Ultrasonic synthesis of stable, functional lysozyme microbubbles Langmuir 2008, 24, 10078-10083
25. Vargo, K. B.; Sood, N.; Moeller, T.; Heiney, P.; Hammer, D. A. Spherical micelles assembled from soluble recombinant olesoin mutants. Langmuir 2014, 30, 11292 - 11300.
26. Xia, Y.; Whitesides, G. M. Soft lithography Angew. Chem., Int. Ed. 1998, 37, 550-575
27. Dhanaliwala, A. H.; Chen, J. L.; Wang, S.; Hossack, J. A. Liquid flooded flow-focusing microfluidic device for in situ generation of monodisperse microbubbles Microfluid. Nanofluid. 2013, 14, 457-467
28. Abate, A. R.; Romanowsky, M. B.; Agresti, J. J.; Weitz, D. A. Valve-based flow focusing for drop formation Appl. Phys. Lett. 2009, 94, 023503
29. Tu, F.; Lee, D. Controlling the stability and size of double-emulsion-templated poly(lactic-co-glycolic) acid microcapsules Langmuir 2012, 28, 9944-9952
30. Erb, R. M.; Obrist, D.; Chen, P. W.; Studer, J.; Studart, A. R. Predicting sizes of droplets made by microfluidic flow-induced dripping Soft Matter 2011, 7, 8757-8761
31. Alexander, L.; Sessions, R.; Clarke, A.; Tatham, A.; Shewry, P.; Napier, J. Characterization and modelling of the hydrophobic domain of a sunflower oleosin Planta 2002, 214, 546-551
32. Peng, C.-C.; Lee, V. S. Y.; Lin, M.-Y.; Huang, H.-Y.; Tzen, J. T. C. Minimizing the central hydrophobic domain in oleosin for the constitution of artificial oil bodies J. Agric. Food Chem. 2007, 55, 5604-5610
33. Bhatla, S.; Kaushik, V.; Yadav, M. Use of oil bodies and oleosins in recombinant protein production and other biotechnological applications Biotechnol. Adv. 2010, 28, 293-300
34. Chang, M.-T.; Tsai, T.-R.; Lee, C.-Y.; Wei, Y.-S.; Chen, Y.-J.; Chen, C.-R.; Tzen, J. T. C. Elevating bioavailability of curcumin via encapsulation with a novel formulation of artificial oil bodies J. Agric. Food Chem. 2013, 61, 9666-9671
35. Chiang, C.-J.; Lin, C.-C.; Lu, T.-L.; Wang, H.-F. Functionalized nanoscale oil bodies for targeted delivery of a hydrophobic drug Nanotechnology 2011, 22, 415102
36. Chiang, C.-J.; Lin, L.-J.; Lin, C.-C.; Chang, C.-H.; Chao, Y.-P. Selective internalization of self-assembled artificial oil bodies by HER2/neu -positive cells Nanotechnology 2011, 22, 015102
37. Peng, C.-C.; Chen, J. C.; Shyu, D. J.; Chen, M.-J.; Tzen, J. T. A system for purification of recombinant proteins in Escherichia coli via artificial oil bodies constituted with their oleosin-fused polypeptides J. Biotechnol. 2004, 111, 51-57
38. Shih, R.; Bardin, D.; Martz, T.; Sheeran, P.; Dayton, P. A.; Lee, A. P. Flow-focusing regimes for accelerated production of monodisperse drug-loadable microbubbles toward clinical-scale applications Lab Chip 2013, 13, 4816-4826
39. Schmolka, I. R. Artificial skin I. Preparation and properties of pluronic F-127 gels for treatment of burns J. Biomed. Mater. Res. 1972, 6, 571-582
40. Park, J. I.; Jagadeesan, D.; Williams, R.; Oakden, W.; Chung, S.; Stanisz, G. J.; Kumacheva, E. Microbubbles loaded with nanoparticles: a route to multiple imaging modalities ACS Nano 2010, 4, 6579-6586
41. Park, J. I.; Nie, Z.; Kumachev, A.; Kumacheva, E. Small, stable, and monodispersed bubbles encapsulated with biopolymers Soft Matter 2010, 6, 630-634
42. Dressaire, E.; Bee, R.; Bell, D. C.; Lips, A.; Stone, H. A. Interfacial polygonal nanopatterning of stable microbubbles Science 2008, 320, 1198-1201
43. Lee, M. H.; Lee, D. Elastic instability of polymer-shelled bubbles formed from air-in-oil-in-water compound bubbles Soft Matter 2010, 6, 4326-4330
44. Lee, M. H.; Prasad, V.; Lee, D. Microfluidic fabrication of stable nanoparticle-shelled bubbles Langmuir 2010, 26, 2227-2230
45. Straub, J. A.; Chickering, D. E.; Church, C. C.; Shah, B.; Hanlon, T.; Bernstein, H. Porous PLGA microparticles: AI-700, an intravenously administered ultrasound contrast agent for use in echocardiography J. Controlled Release 2005, 108, 21-32
46. Eisenbrey, J. R.; Hsu, J.; Wheatley, M. A. Plasma sterilization of poly lactic acid ultrasound contrast agents: surface modification and implications for drug delivery Ultrasound Med. Biol. 2009, 35, 1854-1862
47. Eisenbrey, J.; Burstein, O. M.; Wheatley, M. Effect of molecular weight and end capping on poly(lactic-co-glycolic acid) ultrasound contrast agents Polym. Eng. Sci. 2008, 48, 1785-1792
48. Leodore, L.; Oum, K.; Lathia, J.; Wheatley, M. Surface modification of a polymeric contrast agent for cancer targeting IEEE Annu. Northeast Bioeng. Conf., 31st 2005, 142-143
49. El-Sherif, D. M.; Lathia, J. D.; Le, N. T.; Wheatley, M. A. Ultrasound degradation of novel polymer contrast agents J. Biomed. Mater. Res., Part A 2004, 68A, 71-78
50. Narayan, P.; Wheatley, M. A. Preparation and characterization of hollow microcapsules for use as ultrasound contrast agents Polym. Eng. Sci. 1999, 39, 2242-2255
51. Schrope, B.; Shen, P.; Wheatley, M. Polymeric systems for diagnostic ultrasound contrast agents Cosmet. Pharm. Appl. Polym. 1991, 371-384
52. Singhal, S.; Moser, C. C.; Wheatley, M. A. Surfactant-stabilized microbubbles as ultrasound contrast agents: stability study of Span 60 and Tween 80 mixtures using a Langmuir trough Langmuir 1993, 9, 2426-2429
53. Borden, M.; Sirsi, S.; Hernandez, S.; Homma, S.; Kandel, J.; Yamashiro, D. Polyplex-microbubbles for improved ultrasound-mediated gene therapy J. Acoust. Soc. Am. 2013, 133, 3409-3409
54. Geers, B.; De Wever, O.; Demeester, J.; Bracke, M.; De Smedt, S. C.; Lentacker, I. Targeted liposome-loaded microbubbles for cell-specific ultrasound-triggered drug delivery Small 2013, 9, 4027-4035
55. Park, Y.; Luce, A. C.; Whitaker, R. D.; Amin, B.; Cabodi, M.; Nap, R. J.; Szleifer, I.; Cleveland, R. O.; Nagy, J. O.; Wong, J. Y. Tunable diacetylene polymerized shell microbubbles as ultrasound contrast agents Langmuir 2012, 28, 3766-3772
56. Seo, M.; Gorelikov, I.; Williams, R.; Matsuura, N. Microfluidic assembly of monodisperse, nanoparticle-incorporated perfluorocarbon microbubbles for medical imaging and therapy Langmuir 2010, 26, 13855-13860
57. Wan, J.; Stone, H. A. Lipid monolayer dilatational mechanics during microbubble gas exchange Langmuir 2012, 28, 37-41
58. Chen, H.; Li, J.; Wan, J.; Weitz, D. A.; Stone, H. A. Gas-core triple emulsions for ultrasound triggered release Soft Matter 2013, 9, 38-42
59. Zha, Z.; Wang, J.; Qu, E.; Zhang, S.; Jin, Y.; Wang, S.; Dai, Z. Polypyrrole hollow microspheres as echogenic photothermal agent for ultrasound imaging guided tumor ablation Sci. Rep. 2013, 3, 2360
60. Garg, S.; Thomas, A. A.; Borden, M. A. The effect of lipid monolayer in-plane rigidity on in vivo microbubble circulation persistence Biomaterials 2013, 34, 6862-6870
61. A bright spot in the center of each microbubble, we believe, is due to an artifact of confocal microscopy. Similar bright spots have been observed and attributed to an artifact due to reflection in previous reports (Masters, B. R.; Paddock, S. W. Confocal bioimaging the living cornea with autofluorescence and specific fluorescent probes. Bioimaging and Two-Dimensional Spectroscopy, 1990; Proc. SPIE 1205, 164.
62. Masters, B. R. Confocal microscopy of the eye. New Methods in Microscopy and Low Light Imaging, 1989; Proc. SPIE 1161, 350.
63. Sehgal, C. M.; Cary, T. W.; Arger, P. H.; Wood, A. K. W. Delta projection imaging on contrast-enhanced ultrasound to quantify tumor microvasculature and perfusion Acad. Radiol. 2009, 16, 71-78