Protection and Delivery of Anthelmintic Protein Cry5B to Nematodes Using Mesoporous Silicon Particles

ACS Nano

Volumn 9, Issue 6, 2015, Pages 6158-6167

  Wu, Chia Chen ^a   Hu, Yan ^b   Miller, Melanie ^b   Aroian, Raffi V ^b   Sailor, Michael J ^a,c  

^a Materials Science and Engineering   (United States)

^b Section of Cell and Development Biology   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

A. ceylanicum; Bacillus thuringiensis (Bt); C. elegans; crystal protein; hookworm; oral drug delivery; porous silicon

Indexed keywords

BACTERIOLOGY; PARTICLE SIZE; POROUS SILICON; SILICON; TOXICITY;

A. CEYLANICUM; BACILLUS THURINGIENSIS; CRYSTAL PROTEINS; ELEGANS; HOOKWORM; ORAL DRUG DELIVERY;

PROTEINS;

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; NANOMATERIAL; SILICON;

ANCYLOSTOMA; ANIMAL; CAENORHABDITIS ELEGANS; CHEMISTRY; DRUG EFFECTS; DRUG SENSITIVITY; HAMSTER; NEMATODE; PARASITOLOGY; PARTICLE SIZE; POROSITY; SURFACE PROPERTY;

ANCYLOSTOMA; ANIMALS; BACTERIAL PROTEINS; CAENORHABDITIS ELEGANS; CRICETINAE; ENDOTOXINS; HEMOLYSIN PROTEINS; NANOSTRUCTURES; NEMATODA; PARASITIC SENSITIVITY TESTS; PARTICLE SIZE; POROSITY; SILICON; SURFACE PROPERTIES;

EID: 84934948465     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b01426     Document Type: Article

References (61)

1. Ojha, S. C.; Jaide, C.; Jinawath, N.; Rotjanapan, P.; Baral, P. Geohelminths: Public Health Significance J. Infect. Dev. Countries 2014, 8, 005-016
2. Bleakley, H. Disease and Development: Evidence From Hookworm Eradication in the American South Q. J. Econ. 2007, 122, 73-117
3. Humphries, D.; Simms, B. T.; Davey, D.; Otchere, J.; Quagraine, J.; Terryah, S.; Newton, S.; Berg, E.; Harrison, L. M.; Boakye, D.; Wilson, M.; Cappello, M. Hookworm Infection among School Age Children in Kintampo North Municipality, Ghana: Nutritional Risk Factors and Response to Albendazole Treatment Am. J. Trop. Med. Hyg. 2013, 89, 540-548
4. Geary, T. G. Are New Anthelmintics Needed to Eliminate Human Helminthiases? Curr. Opin. Infect. Dis. 2012, 25, 709-717
5. Whalon, M. E.; Wingerd, B. A. Bt: Mode of Action and Use Arch. Insect Biochem. Physiol. 2003, 54, 200-211
6. Urban, J. F. J.; Hu, Y.; Miller, M. M.; Scheib, U.; Yiu, Y. Y.; Aroian, R. V. Bacillus thuringiensis-Derived Cry5B Has Potent Anthelmintic Activity Against Ascaris suum PLoS Neglected Trop. Dis. 2013, 7, e2263
7. Hu, Y.; Aroian, R. V. Bacterial Pore-Forming Proteins as Anthelmintics Invertebr. Neurosci. 2012, 12, 37-41
8. Hu, Y.; Aroian, R. V., Promise of Bacillus thuringiensis Crystal Proteins as Anthelmintics. In Parasitic Helminths: Targets, Screens, Drugs and Vaccines; Caffrey, C. R., Ed.; Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany, 2012; pp 267-281.
9. Canham, L. T. Bioactive Silicon Structure Fabrication Through Nanoetching Techniques Adv. Mater. 1995, 7, 1033-1037
10. Anderson, S. H. C.; Elliott, H.; Wallis, D. J.; Canham, L. T.; Powell, J. J. Dissolution of Different Forms of Partially Porous Silicon Wafers Under Simulated Physiological Conditions Phys. Status Solidi A 2003, 197, 331-335
11. Low, S. P.; Voelcker, N. H.; Canham, L. T.; Williams, K. A. The Biocompatibility of Porous Silicon in Tissues of the Eye Biomaterials 2009, 30, 2873-2880
12. Canham, L. T.; Stewart, M. P.; Buriak, J. M.; Reeves, C. L.; Anderson, M.; Squire, E. K.; Allcock, P.; Snow, P. A. Derivatized Porous Silicon Mirrors: Implantable Optical Components With Slow Resorbability Phys. Status Solidi A 2000, 182, 521-5
13. Anglin, E. J.; Cheng, L.; Freeman, W. R.; Sailor, M. J. Porous silicon in drug delivery devices and materials Adv. Drug Delivery Rev. 2008, 60, 1266-1277
14. Salonen, J.; Kaukonen, A. M.; Hirvonen, J.; Lehto, V. P. Mesoporous Silicon in Drug Delivery Applications J. Pharm. Sci. 2008, 97, 632-653
15. Holden-Dye, L.; Walker, R. J. Anthelmintic Drugs. In WormBook; The C. elegans Research Community, Ed.; WormBook, 2007. DOI: 10.1895/wormbook.1.143.1. http://www.wormbook.org.
16. Xia, L.-Q.; Zhao, X.-M.; Ding, X.-Z.; Wang, F.-X.; Sun, Y.-J. The Theoretical 3D Structure of Bacillus thuringiensis Cry5Ba J. Mol. Model 2008, 14, 843-848
17. Hui, F.; Scheib, U.; Hu, Y.; Sommer, R. J.; Aroian, R. V.; Ghosh, P. Structure and Glycolipid Binding Properties of the Nematicidal Protein Cry5B Biochemistry 2012, 51, 9911-21
18. Collins, B. E.; Dancil, K.-P.; Abbi, G.; Sailor, M. J. Determining Protein Size Using an Electrochemically Machined Pore Gradient in Silicon Adv. Funct. Mater. 2002, 12, 187-191
19. Karlsson, L. M.; Schubert, M.; Ashkenov, N.; Arwin, H. Protein Adsorption in Porous Silicon Gradients Monitored by Spatially Resolved Spectroscopic Ellipsometry Thin Solid Films 2004, 455-456, 726-730
20. DeLouise, L. A.; Kou, P. M.; Miller, B. L. Cross-Correlation of Optical Microcavity Biosensor Response With Immobilized Enzyme Activity. Insights Into Biosensor Sensitivity Anal. Chem. 2005, 77, 3222-3230
21. Park, J. S.; Lim, S. H.; Sim, S. J.; Chae, H.; Yoon, H. C.; Yang, S. S.; Kim, B. W. Enhancement of Sensitivity in Interferometric Biosensing by Using a New Biolinker and Prebinding Antibody J. Microbiol. Biotechnol. 2006, 16, 1968-1976
22. Orosco, M. M.; Pacholski, C.; Sailor, M. J. Real-Time Monitoring of Enzyme Activity in a Mesoporous Silicon Double Layer Nat. Nanotechnol. 2009, 4, 255-258
23. Andrew, J. S.; Anglin, E. J.; Wu, E. C.; Chen, M. Y.; Cheng, L.; Freeman, W. R.; Sailor, M. J. Sustained Release of a Monoclonal Antibody from Electrochemically Prepared Mesoporous Silicon Oxide Adv. Funct. Mater. 2010, 20, 4168-4174
24. Chen, M. Y.; Klunk, M. D.; Diep, V. M.; Sailor, M. J. Electric Field Assisted Protein Transport, Capture, and Interferometric Sensing in Carbonized Porous Silicon Films Adv. Mater. 2011, 23, 4537-4542
25. Prestidge, C. A.; Barnes, T. J.; Mierczynska-Vasilev, A.; Skinner, W.; Peddie, F.; Barnett, C. Loading and Release of a Model Protein From Porous Silicon Powders Phys. Status Solidi A 2007, 204, 3361-3366
26. De Stefano, L.; D'Auria, S. Confocal Imaging of Protein Distributions in Porous Silicon Optical Structures J. Phys.: Condens. Matter 2007, 19, 395009
27. Tay, L.; Rowell, N. L.; Lockwood, D. J.; Boukherroub, R. In Situ Monitoring of Protein Adsorption on Functionalized Porous Si Surfaces J. Vac. Sci. Technol., A 2006, 24, 747-751
28. DeLouise, L. A.; Miller, B. L. Enzyme Immobilization in Porous Silicon: Quantitative Analysis of the Kinetic Parameters for Glutathione-S-Transferases Anal. Chem. 2005, 77, 1950-1956
29. Foraker, A. B.; Walczak, R. J.; Cohen, M. H.; Boiarski, T. A.; Grove, C. F.; Swaan, P. W. Microfabricated Porous Silicon Particles Enhance Paracellular Delivery of Insulin Across Intestinal Caco-2 Cell Monolayers Pharm. Res. 2003, 20, 110-116
30. Arwin, H.; Gavutis, M.; Gustafsson, J.; Schultzberg, M.; Zangooie, S.; Tengvall, P. Protein Adsorption in Thin Porous Silicon Layers Phys. Status Solidi A 2000, 182, 515-20
31. Zangooie, S.; Bjorklund, R.; Arwin, H. Protein Adsorption in Thermally Oxidized Porous Silicon Layers Thin Solid Films 1998, 313-314, 825-830
32. Chen, M. Y.; Sailor, M. J. Charge-Gated Transport of Proteins in Nanostructured Optical Films of Mesoporous Silica Anal. Chem. 2011, 83, 7186-7193
33. Sailor, M. J. Porous Silicon in Practice: Preparation, Characterization, and Applications; Wiley-VCH: Weinheim, Germany, 2012; p 249.
34. Canham, L. T. Nanoscale Semiconducting Silicon as a Nutritional Food Additive Nanotechnology 2007, 18, 185704
35. Wu, E. C.; Andrew, J. S.; Buyanin, A.; Kinsella, J. M.; Sailor, M. J. Suitability of Porous Silicon Microparticles for the Long-Term Delivery of Redox-Active Therapeutics Chem. Commun. 2011, 47, 5699-5701
36. Park, J.-H.; Gu, L.; Maltzahn, G. v.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Biodegradable Luminescent Porous Silicon Nanoparticles for in vivo Applications Nat. Mater. 2009, 8, 331-336
37. Cheng, L.; Anglin, E.; Cunin, F.; Kim, D.; Sailor, M. J.; Falkenstein, I.; Tammewar, A.; Freeman, W. R. Intravitreal Properties of Porous Silicon Photonic Crystals: a Potential Self-Reporting Intraocular Drug Delivery Vehicle Br. J. Ophthalmol. 2008, 92, 705-711
38. Schwartz, M. P.; Derfus, A. M.; Alvarez, S. D.; Bhatia, S. N.; Sailor, M. J. The Smart Petri Dish: A Nanostructured Photonic Crystal for Real-Time Monitoring of Living Cells Langmuir 2006, 22, 7084-7090
39. Mayne, A. H.; Bayliss, S. C.; Barr, P.; Tobin, M.; Buckberry, L. D. Biologically Interfaced Porous Silicon Devices Phys. Status Solidi A 2000, 182, 505-13
40. Bayliss, S. C.; Buckberry, L. D.; Harris, P. J.; Tobin, M. Nature of the Silicon-Animal Cell Interface J. Porous Mater. 2000, 7, 191-195
41. Canham, L. T. Porous silicon as a therapeutic biomaterial. In Proceedings of 1st Annual International IEEE-EMBS Special Topic Conference on Microtechnologies in Medicine and Biology, Lyon, France, October 12-14, 2000; pp 109-112.
42. Schwartz, M. P.; Yu, C.; Alvarez, S. D.; Migliori, B.; Godin, D.; Chao, L.; Sailor, M. J. Using an Oxidized Porous Silicon Interferometer for Determination of Relative Protein Binding Affinity Through Non-Covalent Capture Probe Immobilization Phys. Status Solidi A 2007, 204, 1444-1448
43. Bonanno, L. M.; DeLouise, L. A. Steric Crowding Effects on Target Detection in an Affinity Biosensor Langmuir 2007, 23, 5817-5823
44. Tsargorodskaya, A.; Nabok, A. V.; Ray, A. K. Ellipsometric Study of the Adsorption of Bovine Serum Albumin into Porous Silicon Nanotechnology 2004, 15, 703-709
45. Wu, E. C.; Andrew, J. S.; Cheng, L.; Freeman, W. R.; Pearson, L.; Sailor, M. J. Real-Time Monitoring of Sustained Drug Release Using the Optical Properties of Porous Silicon Photonic Crystal Particles Biomaterials 2011, 32, 1957-1966
46. Clokey, G. V.; Jacobson, L. A. The Autofluorescent "Lipofuscin Granules" in the Intestinal Cells of Caenorhabditis elegans are Secondary Lysosomes Mech. Ageing Dev. 1986, 35, 79-94
47. Pluskota, A.; Horzowski, E.; Bossinger, O.; von Mikecz, A. In Caenorhabditis elegans Nanoparticle-Bio-Interactions Become Transparent: Silica-Nanoparticles Induce Reproductive Senescence PLoS One 2009, 4, e6622
48. Inpankaew, T.; Schär, F.; Dalsgaard, A.; Khieu, V.; Chimnoi, W.; Chhoun, C.; Sok, D.; Marti, H.; Muth, S.; Odermatt, P.; Traub, R. J. High Prevalence of Ancylostoma ceylanicum Hookworm Infections in Humans, Cambodia, 2012 Emerging Infect. Dis. 2014, 20, 976-82
49. Hu, Y.; Zhan, B.; Keegan, B.; Yiu, Y. Y.; Miller, M. M.; Jones, K.; Aroian, R. V. Mechanistic and Single-Dose in vivo Therapeutic Studies of Cry5B Anthelmintic Action Against Hookworms PLoS Neglected Trop. Dis. 2012, 6, e1900
50. Hu, Y.; Ellis, B. L.; Yiu, Y. Y.; Miller, M. M.; Urban, J. F.; Shi, L. Z.; Aroian, R. V. An Extensive Comparison of the Effect of Anthelmintic Classes on Diverse Nematodes PLoS One 2013, 8, e70702
51. Weitschies, W.; Kosch, O.; Mönnikes, H.; Trahms, L. Magnetic Marker Monitoring: An Application of Biomagnetic Measurement Instrumentation and Principles for the Determination of the Gastrointestinal Behavior of Magnetically Marked Solid Dosage Forms Adv. Drug Delivery Rev. 2005, 57, 1210-1222
52. Ponchel, G.; Irache, J.-M. Specific and Non-specific Bioadhesive Particulate Systems for Oral Delivery to the Gastrointestinal Tract Adv. Drug Delivery Rev. 1998, 34, 191-219
53. Cappello, M.; Bungiro, R. D.; Harrison, L. M.; Bischof, L. J.; Griffitts, J. S.; Barrows, B. D.; Aroian, R. V. A Purified Bacillus thuringiensis Crystal Protein With Therapeutic Activity Against the Hookworm Parasite Ancylostoma ceylanicum Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 15154-15159
54. Griffitts, J. S.; Whitacre, J. L.; Stevens, D. E.; Aroian, R. V. Bt Toxin Resistance From Loss of a Putative Carbohydrate-Modifying Enzyme Science 2001, 293, 860-864
55. Qin, Z.; Joo, J.; Gu, L.; Sailor, M. J. Size Control of Porous Silicon Nanoparticles by Electrochemical Perforation Etching Part. Part. Syst. Charact. 2014, 31, 252-256
56. Bimbo, L. M.; Sarparanta, M.; Santos, H. A.; Airaksinen, A. J.; Mäkilä, E.; Laaksonen, T.; Peltonen, L.; Lehto, V.-P.; Hirvonen, J.; Salonen, J. Biocompatibility of Thermally Hydrocarbonized Porous Silicon Nanoparticles and their Biodistribution in Rats ACS Nano 2010, 4, 3023-3032
57. Meade, S. O.; Chen, M. Y.; Sailor, M. J.; Miskelly, G. M. Multiplexed DNA Detection Using Spectrally Encoded Porous SiO2 Photonic Crystal Particles Anal. Chem. 2009, 81, 2618-2625
58. Hu, Y.; Xiao, S.-H.; Aroian, R. V. The New Anthelmintic Tribendimidine is an L-type (Levamisole and Pyrantel) Nicotinic Acetylcholine Receptor Agonist PLoS Neglected Trop. Dis. 2009, 3, e499
59. Hu, Y.; Georghiou, S. B.; Kelleher, A. J.; Aroian, R. V. Bacillus thuringiensis Cry5B protein is highly efficacious as a single-dose therapy aginst an intestinal roundworm infection in mice PLoS Neglected Trop. Dis. 2010, 4, e614
60. Bischof, L. J.; Huffman, D. L.; Aroian, R. V., Assays for Toxicity Studies in C. elegans With Bt Crystal Proteins. In C. elegans: Methods and Applications, Strange, K., Ed.; Springer: Switzerland, 2006; Vol. 351, pp 139-154.
61. Kao, C. Y.; Los, F. C. O.; Huffman, D. L.; Wachi, S.; Kloft, N.; Husmann, M.; Karabrahimi, V.; Schwartz, J. L.; Bellier, A.; Ha, C.; Sagong, Y.; Fan, H.; Ghosh, P.; Hsieh, M.; Hsu, C. S.; Chen, L.; Aroian, R. V. Global Functional Analyses of Cellular Responses to Pore-Forming Toxins PLoS Pathog. 2011, 7, 17