Interactions of microbicide nanoparticles with a simulated vaginal fluid

Molecular Pharmaceutics

Volumn 9, Issue 11, 2012, Pages 3347-3356

  Das Neves, José ^a,b   Rocha, Cristina M R ^a   Gonçalves, Maria Pilar ^a   Carrier, Rebecca L ^c   Amiji, Mansoor ^d   Bahia, Maria Fernanda ^a   Sarmento, Bruno ^a,b,e  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY INSTITUTE OF HEALTH SCIENCES IUCS   (Portugal)

^c Northeastern University   (United States)

^d NORTHEASTERN UNIVERSITY   (United States)

^e INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

Author keywords

microbicides; mucin; mucoadhesion; mucosal drug delivery; particle tracking; rheology

Indexed keywords

CETRIMIDE; DAPIVIRINE; DODECYL SULFATE SODIUM; MICROBICIDE; MUCIN; NANOCARRIER; NANOPARTICLE; PACLITAXEL; POLYCAPROLACTONE;

ARTICLE; BODY FLUID; CHEMICAL INTERACTION; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; FLOW KINETICS; PARTICLE SIZE; PARTICLE TRACKING; PH; PRIORITY JOURNAL; SIMULATED VAGINAL FLUID; UTERINE CERVIX MUCUS; VAGINA DISCHARGE;

ANTI-INFECTIVE AGENTS; BIOLOGICAL TRANSPORT; BODY FLUIDS; CETRIMONIUM COMPOUNDS; DIFFUSION; DRUG DELIVERY SYSTEMS; FEMALE; HIV REVERSE TRANSCRIPTASE; HUMANS; MUCUS; NANOPARTICLES; PARTICLE SIZE; POLOXAMER; POLYESTERS; PYRIMIDINES; SODIUM DODECYL SULFATE; SURFACE PROPERTIES; TISSUE DISTRIBUTION; VAGINA; WATER;

EID: 84868526145     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300408m     Document Type: Article

References (65)

1. Abdool Karim, Q.; Abdool Karim, S. S.; Frohlich, J. A.; Grobler, A. C.; Baxter, C.; Mansoor, L. E.; Kharsany, A. B.; Sibeko, S.; Mlisana, K. P.; Omar, Z.; Gengiah, T. N.; Maarschalk, S.; Arulappan, N.; Mlotshwa, M.; Morris, L.; Taylor, D. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women Science 2010, 329, 1168-1174
2. Ariën, K. K.; Jespers, V.; Vanham, G. HIV sexual transmission and microbicides Rev. Med. Virol. 2011, 21, 110-133
3. Rohan, L. C.; Sassi, A. B. Vaginal drug delivery systems for HIV prevention AAPS J. 2009, 11, 78-87
4. das Neves, J.; Amiji, M. M.; Bahia, M. F.; Sarmento, B. Nanotechnology-based systems for the treatment and prevention of HIV/AIDS Adv. Drug Delivery Rev. 2010, 62, 458-477
5. das Neves, J.; Bahia, M. F.; Amiji, M. M.; Sarmento, B. Mucoadhesive nanomedicines: characterization and modulation of mucoadhesion at the nanoscale Expert Opin. Drug Delivery 2011, 8, 1085-1104
6. Cone, R. A. Barrier properties of mucus Adv. Drug Delivery Rev. 2009, 61, 75-85
7. Ensign, L. M.; Cone, R.; Hanes, J. Oral drug delivery with polymeric nanoparticles: the gastrointestinal mucus barriers Adv. Drug Delivery Rev. 2012, 64, 557-570
8. das Neves, J.; Amiji, M.; Sarmento, B. Mucoadhesive nanosystems for vaginal microbicide development: friend or foe? Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2011, 3, 389-399
9. Suh, J.; Wirtz, D.; Hanes, J. Efficient active transport of gene nanocarriers to the cell nucleus Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 3878-3882
10. Suk, J. S.; Lai, S. K.; Wang, Y. Y.; Ensign, L. M.; Zeitlin, P. L.; Boyle, M. P.; Hanes, J. The penetration of fresh undiluted sputum expectorated by cystic fibrosis patients by non-adhesive polymer nanoparticles Biomaterials 2009, 30, 2591-2597
11. Crater, J. S.; Carrier, R. L. Barrier properties of gastrointestinal mucus to nanoparticle transport Macromol. Biosci. 2010, 10 (12) 1473-1483
12. Dawson, M.; Krauland, E.; Wirtz, D.; Hanes, J. Transport of polymeric nanoparticle gene carriers in gastric mucus Biotechnol. Prog. 2004, 20, 851-857
13. Lieleg, O.; Vladescu, I.; Ribbeck, K. Characterization of particle translocation through mucin hydrogels Biophys. J. 2010, 98, 1782-1789
14. Lai, S. K.; OHanlon, D. E.; Harrold, S.; Man, S. T.; Wang, Y. Y.; Cone, R.; Hanes, J. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 1482-1487
15. Tang, B. C.; Dawson, M.; Lai, S. K.; Wang, Y. Y.; Suk, J. S.; Yang, M.; Zeitlin, P.; Boyle, M. P.; Fu, J.; Hanes, J. Biodegradable polymer nanoparticles that rapidly penetrate the human mucus barrier Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 19268-19273
16. Suh, J.; Dawson, M.; Hanes, J. Real-time multiple-particle tracking: applications to drug and gene delivery Adv. Drug Delivery Rev. 2005, 57, 63-78
17. Wang, Y. Y.; Lai, S. K.; Suk, J. S.; 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. 2008, 47, 9726-9729
18. Cu, Y.; Saltzman, W. M. Controlled surface modification with poly(ethylene)glycol enhances diffusion of PLGA nanoparticles in human cervical mucus Mol. Pharmaceutics 2009, 6, 173-181
19. Yang, M.; Lai, S. K.; Wang, Y. Y.; Zhong, W.; Happe, C.; Zhang, M.; Fu, J.; Hanes, J. Biodegradable nanoparticles composed entirely of safe materials that rapidly penetrate human mucus Angew. Chem., Int. Ed. 2011, 50, 2597-2600
20. Ensign, L. M.; Tang, B. C.; Wang, Y. Y.; Tse, T. A.; Hoen, T.; Cone, R.; Hanes, J. Mucus-penetrating nanoparticles for vaginal drug delivery protect against herpes simplex virus Sci. Transl. Med. 2012, 4, 138ra79
21. Alexis, F.; Pridgen, E.; Molnar, L. K.; Farokhzad, O. C. Factors affecting the clearance and biodistribution of polymeric nanoparticles Mol. Pharmaceutics 2008, 5, 505-515
22. Zahr, A. S.; Davis, C. A.; Pishko, M. V. Macrophage uptake of core-shell nanoparticles surface modified with poly(ethylene glycol) Langmuir 2006, 22, 8178-8185
23. das Neves, J.; Michiels, J.; Arien, K. K.; Vanham, G.; Amiji, M.; Bahia, M. F.; Sarmento, B. Polymeric nanoparticles affect the intracellular delivery, antiretroviral activity and cytotoxicity of the microbicide drug candidate dapivirine Pharm. Res. 2012, 29, 1468-1484
24. das Neves, J.; Sarmento, B.; Amiji, M. M.; Bahia, M. F. Development and validation of a rapid reversed-phase HPLC method for the determination of the non-nucleoside reverse transcriptase inhibitor dapivirine from polymeric nanoparticles J. Pharm. Biomed. Anal. 2010, 52, 167-172
25. Owen, D. H.; Katz, D. F. A vaginal fluid simulant Contraception 1999, 59, 91-95
26. Lee, C. H.; Wang, Y.; Shin, S. C.; Chien, Y. W. Effects of chelating agents on the rheological property of cervical mucus Contraception 2002, 65, 435-440
27. Vermani, K.; Garg, S.; Zaneveld, L. J. Assemblies for in vitro measurement of bioadhesive strength and retention characteristics in simulated vaginal environment Drug Dev. Ind. Pharm. 2002, 28, 1133-1146
28. das Neves, J.; Amaral, M. H.; Bahia, M. F. Performance of an in vitro mucoadhesion testing method for vaginal semisolids: Influence of different testing conditions and instrumental parameters Eur. J. Pharm. Biopharm. 2008, 69, 622-632
29. Takeuchi, H.; Thongborisute, J.; Matsui, Y.; Sugihara, H.; Yamamoto, H.; Kawashima, Y. Novel mucoadhesion tests for polymers and polymer-coated particles to design optimal mucoadhesive drug delivery systems Adv. Drug Delivery Rev. 2005, 57, 1583-1594
30. Grenha, A. Chitosan nanoparticles: a survey of preparation methods J. Drug Targeting 2012, 20, 291-300
31. Bravo-Osuna, I.; Vauthier, C.; Farabollini, A.; Palmieri, G. F.; Ponchel, G. Mucoadhesion mechanism of chitosan and thiolated chitosan-poly(isobutyl cyanoacrylate) core-shell nanoparticles Biomaterials 2007, 28, 2233-2243
32. Sbalzarini, I. F.; Koumoutsakos, P. Feature point tracking and trajectory analysis for video imaging in cell biology J. Struct. Biol. 2005, 151, 182-195
33. Saxton, M. J.; Jacobson, K. Single-particle tracking: applications to membrane dynamics Annu. Rev. Biophys. Biomol. Struct. 1997, 26, 373-399
34. Lai, S. K.; Wang, Y. Y.; Hanes, J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues Adv. Drug Delivery Rev. 2009, 61, 158-171
35. Boskey, E. R.; Telsch, K. M.; Whaley, K. J.; Moench, T. R.; Cone, R. A. Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification Infect. Immun. 1999, 67, 5170-5175
36. Mason, T. G.; Ganesan, K.; van Zanten, J. H.; Wirtz, D.; Kuo, S. C. Particle tracking microrheology of complex fluids Phys. Rev. Lett. 1997, 79, 3282-3285
37. Mason, T. G. Estimating the viscoelastic moduli of complex fluids using the generalized Stokes-Einstein equation Rheol. Acta 2000, 39, 371-378
38. Lai, S. K.; Wang, Y. Y.; Cone, R.; Wirtz, D.; Hanes, J. Altering mucus rheology to "solidify" human mucus at the nanoscale PLoS One 2009, 4, e4294
39. Lai, S. K.; Wang, Y. Y.; Hida, K.; Cone, R.; Hanes, J. Nanoparticles reveal that human cervicovaginal mucus is riddled with pores larger than viruses Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 598-603
40. Shenoy, D. B.; Amiji, M. M. Poly(ethylene oxide)-modified poly(epsilon-caprolactone) nanoparticles for targeted delivery of tamoxifen in breast cancer Int. J. Pharm. 2005, 293, 261-270
41. Shah, L. K.; Amiji, M. M. Intracellular delivery of saquinavir in biodegradable polymeric nanoparticles for HIV/AIDS Pharm. Res. 2006, 23, 2638-2645
42. McGill, S.; Smyth, H. Disruption of the mucus barrier by topically applied exogenous particles Mol. Pharmaceutics 2010, 7, 2280-2288
43. das Neves, J.; Amaral, M. H.; Bahia, M. F. Vaginal Drug Delivery. In Pharmaceutical Manufacturing Handbook: Production and Processes; Gad, S. C., Ed.; Wiley: Hoboken, NJ, 2008; pp 809-878.
44. Lai, S. K.; Hida, K.; Shukair, S.; Wang, Y. Y.; Figueiredo, A.; Cone, R.; Hope, T. J.; Hanes, J. Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus J. Virol. 2009, 83, 11196-11200
45. Cone, R. A. Mucus. In Mucosal Immunology, 3 rd ed.; Mestecky, J.; Lamm, M. E.; Strober, W.; Bienenstock, J.; McGhee, J. R.; Mayer, L., Eds.; Academic Press: San Diego, CA, 2005; pp 49-72.
46. Katz, D. F. Human cervical mucus: research update Am. J. Obstet. Gynecol. 1991, 165, 1984-1986
47. das Neves, J.; da Silva, M. V.; Gonçalves, M. P.; Amaral, M. H.; Bahia, M. F. Rheological properties of vaginal hydrophilic polymer gels Curr. Drug Delivery 2009, 6, 83-92
48. Celli, J. P.; Turner, B. S.; Afdhal, N. H.; Ewoldt, R. H.; McKinley, G. H.; Bansil, R.; Erramilli, S. Rheology of gastric mucin exhibits a pH-dependent sol-gel transition Biomacromolecules 2007, 8, 1580-1586
49. Madsen, F.; Eberth, K.; Smart, J. D. A rheological examination of the mucoadhesive/mucus interaction: the effect of mucoadhesive type and concentration J. Controlled Release 1998, 50, 167-178
50. Kocæevar-Nared, J.; Kristl, J.; Sæmid-Korbar, J. Comparative rheological investigation of crude gastric mucin and natural gastric mucus Biomaterials 1997, 18, 677-681
51. Waigh, T. A.; Papagiannopoulos, A.; Voice, A.; Bansil, R.; Unwin, A. P.; Dewhurst, C. D.; Turner, B.; Afdhal, N. Entanglement coupling in porcine stomach mucin Langmuir 2002, 18, 7188-7195
52. Rossi, S.; Ferrari, F.; Bonferoni, M. C.; Caramella, C. Characterization of chitosan hydrochloride-mucin rheological interaction: influence of polymer concentration and polymer:mucin weight ratio Eur. J. Pharm. Sci. 2001, 12, 479-485
53. Sriamornsak, P.; Wattanakorn, N. Rheological synergy in aqueous mixtures of pectin and mucin Carbohydr. Polym. 2008, 74, 474-481
54. Shen, J.; Wang, Y.; Ping, Q.; Xiao, Y.; Huang, X. Mucoadhesive effect of thiolated PEG stearate and its modified NLC for ocular drug delivery J. Controlled Release 2009, 137, 217-223
55. Boukari, H.; Brichacek, B.; Stratton, P.; Mahoney, S. F.; Lifson, J. D.; Margolis, L.; Nossal, R. Movements of HIV-virions in human cervical mucus Biomacromolecules 2009, 10, 2482-8
56. Broliden, K.; Haase, A. T.; Ahuja, S. K.; Shearer, G. M.; Andersson, J. Introduction: Back to basics: mucosal immunity and novel HIV vaccine concepts J. Intern. Med. 2009, 265, 5-17
57. Celli, J.; Gregor, B.; Turner, B.; Afdhal, N. H.; Bansil, R.; Erramilli, S. Viscoelastic properties and dynamics of porcine gastric mucin Biomacromolecules 2005, 6, 1329-1333
58. Hong, Z.; Chasan, B.; Bansil, R.; Turner, B. S.; Bhaskar, K. R.; Afdhal, N. H. Atomic force microscopy reveals aggregation of gastric mucin at low pH Biomacromolecules 2005, 6, 3458-3466
59. Maleki, A.; Lafitte, G.; Kjoniksen, A. L.; Thuresson, K.; Nystrom, B. Effect of pH on the association behavior in aqueous solutions of pig gastric mucin Carbohydr. Res. 2008, 343, 328-340
60. Bansil, R.; Turner, B. S. Mucin structure, aggregation, physiological functions and biomedical applications Curr. Opin. Colloid Interface Sci. 2006, 11, 164-170
61. Katz, D. F.; Dunmire, E. N. Cervical mucus: problems and opportunities for drug delivery via the vagina and cervix Adv. Drug Delivery Rev. 1993, 11, 385-401
62. Lieleg, O.; Ribbeck, K. Biological hydrogels as selective diffusion barriers Trends Cell Biol. 2011, 21, 543-551
63. Vladescu, I.; Lieleg, O.; Jang, S.; Ribbeck, K. An adsorption chromatography assay to probe bulk particle transport through hydrogels J. Pharm. Sci. 2012, 101, 436-442
64. Ponchel, G.; Montisci, M. J.; Dembri, A.; Durrer, C.; Duchêne, D. Mucoadhesion of colloidal particulate systems in the gastro-intestinal tract Eur. J. Pharm. Biopharm. 1997, 44, 25-31
65. Sakloetsakun, D.; Perera, G.; Hombach, J.; Millotti, G.; Bernkop-Schnürch, A. The impact of vehicles on the mucoadhesive properties of orally administrated nanoparticles: a case study with chitosan-4- thiobutylamidine conjugate AAPS PharmSciTech 2010, 11, 1185-1192