Immobilization of Pseudorabies Virus in Porcine Tracheal Respiratory Mucus Revealed by Single Particle Tracking

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Yang, Xiaoyun ^a   Forier, Katrien ^a   Steukers, Lennert ^a   van Vlierberghe, Sandra ^b   Dubruel, Peter ^b   Braeckmans, Kevin ^a   Glorieux, Sarah ^a   Nauwynck, Hans J ^a  

^a GHENT UNIVERSITY   (Belgium)

^b Polymer Chemistry and Biomaterials Research Group   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

MACROGOL; NANOPARTICLE; WATER;

ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; COMPARATIVE STUDY; CONTROLLED STUDY; DIFFUSION; ELECTRICITY; HYDROPHILICITY; IMMOBILIZATION; IN VITRO STUDY; MICROSCOPY; NONHUMAN; PARTICLE SIZE; PSEUDORABIES HERPETOVIRUS; SINGLE PARTICLE TRACKING MICROSCOPY; SURFACE CHARGE; SWINE; TRACHEA MUCUS; ZETA POTENTIAL;

ANIMALS; HERPESVIRUS 1, SUID; MUCUS; NANOPARTICLES; PSEUDORABIES; RESPIRATORY SYSTEM; SWINE;

SUID HERPESVIRUS 1; SUS;

EID: 84870912120     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051054     Document Type: Article

References (52)

1. Murphy JA, Duerst RJ, Smith TJ, Morrison LA, (2003) Herpes simplex virus type 2 virion host shutoff protein regulates alpha/beta interferon but not adaptive immune responses during primary infection in vivo. J Virol 77(17): 9337-45.
2. Steukers L, Vandekerckhove AP, Van den Broeck W, Glorieux S, Nauwynck HJ, (2011) Comparative analysis of replication characteristics of BoHV-1 subtypes in bovine respiratory and genital mucosa explants: a phylogenetic enlightenment. Vet Res 42(1): 33.
3. Glorieux S, Favoreel HW, Steukers L, Vandekerckhove AP, Nauwynck HJ, (2011) A trypsin-like serine protease is involved in pseudorabies virus invasion through the basement membrane barrier of porcine nasal respiratory mucosa. Vet Res 42(1): 58.
4. Gibson JS, Slater JD, Awan AR, Field HJ, (1992) Pathogenesis of equine herpesvirus-1 in specific pathogen-free foals: primary and secondary infections and reactivation. Arch Virol 123: 351-366.
5. Nauwynck HJ, (1997) Functional aspects of Aujeszky's disease (pseudorabies) viral proteins with relation to invasion, virulence and immunogenicity. Vet Microbiol 55: 3-11.
6. Nauwynck HJ, Glorieux S, Favoreel H, Pensaert M, (2007) Cell biological and molecular characteristics of pseudorabies virus infections in cell cultures and in pigs with emphasis on the respiratory tract. Vet Res 38: 229-241.
7. Maeda K, Horimoto T, Mikami T, (1998) Properties and functions of feline herpesvirus type 1 glycoproteins. J Vet Med Sci 60: 881-888.
8. Glorieux S, Favoreel HW, Meesen G, de Vos W, Van den Broeck W, et al. (2009) Different replication characteristics of historical pseudorabies virus strains in porcine respiratory nasal mucosa explants. Vet Microbiol 136(3-4): 341-6.
9. Vandekerckhove AP, Glorieux S, Gryspeerdt AC, Steukers L, Duchateau L, et al. (2010) Replication kinetics of neurovirulent versus non-neurovirulent equine herpesvirus type 1 strains in equine nasal mucosal explants. J Gen Virol 91(8): 2019-28.
10. Wittmann G, Jakubik J, Ahl R, (1980) Multiplication and distribution of Aujeszky's disease (pseudorabies) virus in vaccinated and nonvaccinated pigs after intranasal infection. Arch Virol 66: 227-240.
11. Sims DE, Horne MM, (1997) Heterogeneity of the composition and thickness of tracheal mucus in rats. Am J Physiol 273(5): 1036-41.
12. Verkman AS, Song Y, Thiagarajah JR, (2003) Role of airway surface liquid and submucosal glands in cystic fibrosis lung disease. Am J Physiol Cell Physiol 284(1): C2-15.
13. Varum FJ, Veiga F, Sousa JS, Basit AW, (2012) Mucus thickness in the gastrointestinal tract of laboratory animals. J Pharm Pharmacol 64(2): 218-27.
14. Thornton DJ, Rousseau K, McGuckin MA, (2008) Structure and function of the polymeric mucins in airways mucus. Annu Rev Physiol 70: 459-86.
15. Lai SK, Wang YY, Wirtz D, Hanes J, (2008) Micro- and macrorheology of mucus. Adv Drug Deliv Rev 61(2): 86-100.
16. Olmsted SS, Padgett JL, Yudin AI, Whaley KJ, Moench TR, et al. (2001) Diffusion of macromolecules and virus-like particles in human cervical mucus. Biophys J 81: 1930-1937.
17. Hida K, Lai SK, Suk JS, Won SY, Boyle MP, et al. (2011) Common Gene Therapy Viral Vectors Do Not Efficiently Penetrate Sputum from Cystic Fibrosis Patients. PLoS ONE 6(5): e19919.
18. Lai SK, Wang YY, Hida K, Cone R, Hanes J, (2010) Nanoparticles reveal that human cervicovaginal mucus is riddled with pores larger than viruses. Proc Natl Acad Sci USA 107: 598-603.
19. Lai SK, Hida K, Shukair S, Wang YY, Figueiredo A, et al. (2009) Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus. J Virol 83(21): 11196-11200.
20. Gadegaard N, (2006) Atomic force microscopy in biology: technology and techniques. Biotech Histochem 81(2-3): 87-97.
21. Ramachandran S, Teran Arce F, Lal R, (2011) Potential role of atomic force microscopy in systems biology. Wiley Interdiscip Rev Syst Biol Med 3(6): 702-16.
22. Lai SK, Wang YY, Wirtz D, Hanes J, (2009) Micro- and macrorheology of mucus. Adv Drug Deliv Rev 61(2): 86-100.
23. Lai SK, Wang YY, Cone R, Wirtz D, Hanes J, (2009) Altering Mucus Rheology to "Solidify" Human Mucus at the Nanoscale. PLoS ONE 4(1): e4294.
24. Suh J, Dawson M, Hanes J, (2005) Real-time multiple-particle tracking: Applications to drug and gene delivery. Adv Drug Deliv Rev 57(1): 63-78.
25. Broughton-Head V, Smith J, Shur J, Shute J, (2007) Actin limits enhancement of nanoparticle diffusion through cystic fibrosis sputum by mucolytics. Pulm Pharmacol Ther 20(6): 708-717.
26. Symens N, Walczak R, Demeester J, Mattaj I, De Smedt SC, et al. (2011) Nuclear Inclusion of Nontargeted and Chromatin-Targeted Polystyrene Beads and Plasmid DNA Containing Nanoparticles. Mol Pharmaceutics 8(5): 1757-1766.
27. Forier K, Messiaen AS, Raemdonck K, Deschout H, Rejman J, et al. (2012) On the transport of nanoparticles in cystic fibrosis sputum and bacterial biofilms by single particle tracking microscopy. Nanomedicine. In press.
28. Braeckmans K, Vercauteren D, Demeester J, De Smedt SC (2010) Single particle tracking. In: Diaspro A, editor. Nanoscopy multidimensional optical fluorescence microscopy. Taylor and Francis.
29. Qian H, Sheetz MP, Elson EL, (1991) Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys J 60(4): 910-921.
30. Saxton MJ, Jacobson K, (1997) Single-Particle Tracking: Applications to Membrane Dynamics. Annu Rev Biophys Biomol Struct 26: 373-99.
31. Xie H, Haliyo DS, Régnier S, (2009) A versatile atomic force microscope for three-dimensional nanomanipulation and nanoassembly. Nanotechnology 20(21): 215-301.
32. Manzenreiter R, Kienberger F, Marcos V, Schilcher K, Krautgartner WD, et al. (2012) Ultrastructural characterization of cystic fibrosis sputum using atomic force and scanning electron microscopy. J Cyst Fibros 11(2): 84-92.
33. Broughton-Head VJ, Smith JR, Shur J, Shute JK, (2007) Actin limits enhancement of nanoparticle diffusion through cystic fibrosis sputum by mucolytics. Pulm Pharmacol Ther 20(6): 708-17.
34. LeBleu VS, Macdonald B, Kalluri R, (2007) Structure and function of basement membranes. Exp Biol Med 232(9): 1121-9.
35. Abrams GA, Schaus SS, Goodman SL, Nealey PF, Murphy CJ, (2000) Nanoscale topography of the corneal epithelial basement membrane and Descemet's membrane of the human. Cornea 19(1): 57-64.
36. Steukers L, Glorieux S, Vandekerckhove AP, Favoreel HW, Nauwynck HJ, (2012) Diverse microbial interactions with the basement membrane barrier. Trends Microbiol 20(3): 147-55.
37. Hanes J, Lai SK, Wang YY, Wirtz D, (2009) Micro- and macrorheology of mucus. Adv Drug Deliv Rev 61(2): 86-100.
38. King M, (1980) Viscoelastic properties of airway mucus. Fed Proc 39(13): 3080-5.
39. Lieleg O, Baumgartel RM, Bausch AR, (2009) Selective filtering of particles by the extracellular matrix: an electrostatic bandpass. Biophys J 97: 1569-1577.
40. Lieleg O, Vladescu I, Ribbeck K, (2010) Characterization of particle translocation through mucin hydrogels. Biophys J 98(9): 1782-9.
41. Norris DA, Sinko PJ, (1997) Effect of size, surface charge, and hydrophobicity on the translocation of polystyrene microspheres through gastrointestinal mucin. J Appl Polym Sci 63: 1481-1492.
42. Cone RA, (2009) Barrier properties of mucus. Adv Drug Deliv Rev 61(2): 75-85.
43. Mortazavi SA, (1995) An in vitro assessment of mucus/mucoadhesive interactions. Int J Pharm 124: 173.
44. McGrane SJ, Mainwaring DE, Cornell HJ, Rix CJ, (2004) The Role of Hydrogen Bonding in Amylose Gelation. Starch 56: 122.
45. Khutoryanskiy VV, (2011) Advances in mucoadhesion and mucoadhesive polymers. Macromol Biosci 11: 748-764.
46. Croyle MA, Yu QC, Wilson JM, (2000) Development of a Rapid Method for the PEGylation of Adenoviruses with Enhanced Transduction and Improved Stability under Harsh Storage Conditions. Hum Gene Ther 11(12): 1713-1722.
47. Croyle MA, Callahan SM, Auricchio A, Schumer G, Linse KD, et al. (2004) PEGylation of a Vesicular Stomatitis Virus G Pseudotyped Lentivirus Vector Prevents Inactivation in Serum. J Virol 78 (2): 912-92.
48. Trybala E, Bergström T, Spillmann D, Svennerholm B, Olofsson S, et al. (1996) Mode of interaction between pseudorabies virus and heparan sulfate/heparin. Virology 218(1): 35-42.
49. Trybala E, Bergström T, Spillmann D, Svennerholm B, Flynn SJ, et al. (1998) Interaction between pseudorabies virus and heparin/heparan sulfate. Pseudorabies virus mutants differ in their interaction with heparin/heparan sulfate when altered for specific glycoprotein C heparin-binding domain. J Biol Chem 273(9): 5047-52.
50. Hampson IN, Kumar S, Gallagher JT, (1984) Heterogeneity of cell-associated and secretory heparan sulphate proteoglycans produced by cultured human neuroblastoma cells. Biochim Biophys Acta 801(2): 306-13.
51. Emery N, Place GA, Dodd S, Lhermitte M, David G, et al. (1995) Mucous and serous secretions of human bronchial epithelial cells in secondary culture. Am J Respir Cell Mol Biol 12(2): 130-141.
52. Agarwal M, King M, Shukla JB, (1994) Mucus gel transport in a simulated cough machine: effects of longitudinal grooves representing spacings between arrays of cilia. Biorheology 31: 11-19.