Permeability of the small intestinal mucus for physiologically relevant studies: Impact of mucus location and ex vivo treatment
Abstract
The small intestinal mucus is a complex colloidal system that coats the intestinal mucosa. It allows passage on nutrients/pharmaceuticals from the gut lumen towards the epithelium, whilst preventing it from direct contact with luminal microorganisms. Mucus collected from intestinal tissue is often used in studies looking at inter-mucosal transport of food particulates, drug carriers, etc. However, detaching the highly hydrated native mucus from the tissue and storing it frozen prior to use may disrupt its physiological microstructure, and thus selective barrier properties. Multiple-particle tracking experiments showed that microstructural organisation of native, jejunal mucus depends on its spatial location in the intestinal mucosa. The inter-villus mucus was less heterogeneous than the mucus covering villi tips in the pig model used. Collecting mucus from tissue and subjecting it to freezing and thawing did not significantly affect (P > 0.05) its permeability to model, sub-micron sized particles, and the microviscosity profile of the mucus reflected the overall profiles recorded for the native mucus in the tissue. This implies the method of collecting and storing mucus is a reliable ex vivo treatment for the convenient planning and performing of mucus-permeability studies that aim to mimic physiological conditions of the transport of molecules/particles in native mucus.
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- Category:
- Articles
- Type:
- artykuły w czasopismach
- Published in:
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Scientific Reports
no. 9,
pages 1 - 12,
ISSN: 2045-2322 - Language:
- English
- Publication year:
- 2019
- Bibliographic description:
- Macierzanka A., Mackie A., Krupa Ł.: Permeability of the small intestinal mucus for physiologically relevant studies: Impact of mucus location and ex vivo treatment// Scientific Reports -Vol. 9,iss. 1 (2019), s.1-12
- DOI:
- Digital Object Identifier (open in new tab) 10.1038/s41598-019-53933-5
- Bibliography: test
-
- Hansson, G. C. Role of mucus layers in gut infection and inflammation. Curr. Opin. Microbiol. 15, 57-62 (2012). open in new tab
- Bäckström, M., Ambort, D., Thomsson, E., Johansson, M. E. V. & Hansson, G. C. Increased understanding of the biochemistry and biosynthesis of MUC2 and other gel-forming mucins through the recombinant expression of their protein domains. Mol. Biotechnol. 54, 250-256 (2013). open in new tab
- Johansson, M. E. V., Sjövall, H. & Hansson, G. C. The gastrointestinal mucus system in health and disease. Nat. Rev. Gastroenterol. Hepatol. 10, 352-361 (2013). open in new tab
- Bajka, B. H., Rigby, N. M., Cross, K. L., Macierzanka, A. & Mackie, A. R. The influence of small intestinal mucus structure on particle transport ex vivo. Colloids Surfaces B Biointerfaces 135, 73-80 (2015). open in new tab
- Round, A. N. et al. Lamellar structures of MUC2-rich mucin: A potential role in governing the barrier and lubricating functions of intestinal mucus. Biomacromolecules 13, 3253-3261 (2012). open in new tab
- Johansson, M. E. V., Larsson, J. M. H. & Hansson, G. C. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc. Natl. Acad. Sci. 108, 4659-4665 (2011). open in new tab
- Atuma, C., Strugala, V., Allen, A. & Holm, L. The adherent gastrointestinal mucus gel layer: Thickness and physical state in vivo. Am. J. Physiol. -Gastrointest. Liver Physiol. 280, 922-929 (2001). open in new tab
- Lentle, R. G. & de Loubens, C. A review of mixing and propulsion of chyme in the small intestine: Fresh insights from new methods. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 185, 369-387 (2015). open in new tab
- Mackie, A. R. et al. Innovative methods and applications in mucoadhesion research. Macromol. Biosci. 17, 1-32 (2017). open in new tab
- Corfield, A. P. Mucins: A biologically relevant glycan barrier in mucosal protection. Biochim. Biophys. Acta -Gen. Subj. 1850, 236-252 (2015). open in new tab
- Corfield, A. P. Mucins and mucosal protection in the gastrointestinal tract: new prospects for mucins in the pathology of gastrointestinal disease. Gut 47, 589-594 (2000). open in new tab
- Macierzanka, A. et al. Transport of particles in intestinal mucus under simulated infant and adult physiological conditions: Impact of mucus structure and extracellular DNA. PLoS One 9, 1-11 (2014). open in new tab
- Georgiades, P., Pudney, P. D. A. A., Thornton, D. J. & Waigh, T. A. Particle tracking microrheology of purified gastrointestinal mucins. Biopolymers 101, 366-377 (2014). open in new tab
- Macierzanka, A. et al. Adsorption of bile salts to particles allows penetration of intestinal mucus. Soft Matter 7, 8077-8084 (2011). open in new tab
- Macierzanka, A. et al. Enzymatically structured emulsions in simulated gastrointestinal environment: Impact on interfacial proteolysis and diffusion in intestinal mucus. Langmuir 28, 17349-17362 (2012). open in new tab
- Sciascia, Q., Daş, G. & Metges, C. C. REVIEW: The pig as a model for humans: Effects of nutritional factors on intestinal function and health. J. Anim. Sci. 94, 441-452 (2016). open in new tab
- Zhang, Q., Widmer, G. & Tzipori, S. A pig model of the human gastrointestinal tract. Gut Microbes 4, 193-200 (2013). open in new tab
- Ensign, L. M. et al. Ex vivo characterization of particle transport in mucus secretions coating freshly excised mucosal tissues. Mol. Pharm. 10, 2176-2182 (2013). open in new tab
- Larhed, A. W., Artursson, P., Gråsjö, J. & Björk, E. Diffusion of drugs in native and purified gastrointestinal mucus. J. Pharm. Sci. 86, 660-665 (1997). open in new tab
- Yildiz, H. M., McKelvey, C. A., Marsac, P. J. & Carrier, R. L. Size selectivity of intestinal mucus to diffusing particulates is dependent on surface chemistry and exposure to lipids. J. Drug Target. 23, 768-774 (2015). open in new tab
- Lagarce, F. et al. Fate of paclitaxel lipid nanocapsules in intestinal mucus in view of their oral delivery. Int. J. Nanomedicine 8, 4291-4302 (2013). open in new tab
- Mackie, A. R. et al. Sodium alginate decreases the permeability of intestinal mucus. Food Hydrocoll. 52, 749-755 (2016). open in new tab
- Mackie, A. et al. The fate of cellulose nanocrystal stabilised emulsions after simulated gastrointestinal digestion and exposure to intestinal mucosa. Nanoscale 11, 2991-2998 (2019). open in new tab
- Bansil, R. & Turner, B. S. Mucin structure, aggregation, physiological functions and biomedical applications. Curr. Opin. Colloid Interface Sci. 11, 164-170 (2006). open in new tab
- Smith, G. W., Wiggins, P. M., Lee, S. P. & Tasman-Jones, C. Diffusion of butyrate through pig colonic mucus in vitro. Clin. Sci. 70, 271-276 (1986). open in new tab
- Bourlieu, C. et al. Specificity of infant digestive conditions: Some clues for developing relevant in vitro models. Crit. Rev. Food Sci. Nutr. 54, 1427-1457 (2014). open in new tab
- Kim, J. & Khan, W. Goblet Cells and Mucins: Role in Innate Defense in Enteric Infections. Pathogens 2, 55-70 (2013). open in new tab
- Hall, P. a., Coates, P. J., Ansari, B. & Hopwood, D. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J. Cell Sci. 107, 563-569 (1994).
- Bullen, T. F. et al. Characterization of epithelial cell shedding from human small intestine. Lab. Investig. 86, 1052-1063 (2006). open in new tab
- Ermund, A., Schütte, A., Johansson, M. E. V., Gustafsson, J. K. & Hansson, G. C. Studies of mucus in mouse stomach, small intestine, and colon. I. Gastrointestinal mucus layers have different properties depending on location as well as over the Peyer's patches. Am. J. Physiol. Liver Physiol. 305, G341-G347 (2013). open in new tab
- Lock, J. Y., Carlson, T. L. & Carrier, R. L. Mucus models to evaluate the diffusion of drugs and particles. Adv. Drug Deliv. Rev. 124, 34-49 (2018). open in new tab
- Varavinit, S., Shobsngob, S., Varanyanond, W., Chinachoti, P. & Naivikul, O. Freezing and thawing conditions affect the gel stability of different varieties of rice flour. Starch/Staerke 54, 31-36 (2002). open in new tab
- Tang, X. et al. Syneresis rate, water distribution, and microstructure of wheat starch gel during freeze-thaw process: Role of a high molecular weight dextran produced by Weissella confusa QS813 from traditional sourdough. Cereal Chem. 95, 117-129 (2018). open in new tab
- Cropotova, J. et al. Effect of freezing on microstructure and degree of syneresis in differently formulated fruit fillings. Food Chem. 195, 71-78 (2016). open in new tab
- Chaplin, M. Do we understanding the importance of water in cell biology? Nat. Rev 7, 861-866 (2006). open in new tab
- Porschke, D. Boundary conditions for free A-DNA in solution and the relation of local to global DNA structures at reduced water activity. Eur. Biophys. J. 45, 413-421 (2016). open in new tab
- Nakano, M. et al. Local thermodynamics of the water molecules around single-and double-stranded DNA studied by grid inhomogeneous solvation theory. Chem. Phys. Lett. 660, 250-255 (2016). open in new tab
- Makarov, V., Pettitt, B. M. & Feig, M. Solvation and hydration of proteins and nucleic acids: A theoretical view of simulation and experiment. Acc. Chem. Res. 35, 376-384 (2002). open in new tab
- Bansil, R. & Turner, B. S. The biology of mucus: Composition, synthesis and organization. Adv. Drug Deliv. Rev. 124, 3-15 (2018). open in new tab
- Taherali, F., Varum, F. & Basit, A. W. A slippery slope: On the origin, role and physiology of mucus. Adv. Drug Deliv. Rev. 124, 16-33 (2018). open in new tab
- Crouzier, T. et al. Modulating mucin hydration and lubrication by deglycosylation and polyethylene glycol binding. Adv. Mater. Interfaces 2, 1-7 (2015). open in new tab
- Lai, S. K., Wang, Y. Y. & Hanes, J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. Adv. Drug Deliv. Rev. 61, 158-171 (2009). open in new tab
- Chu, B. S. et al. Modulating pancreatic lipase activity with galactolipids: Effects of emulsion interfacial composition. Langmuir 25, 9352-9360 (2009). open in new tab
- Mandalari, G., Mackie, A. M., Rigby, N. M., Wickham, M. S. J. & Mills, E. N. C. Physiological phosphatidylcholine protects bovine β-lactoglobulin from simulated gastrointestinal proteolysis. Mol. Nutr. Food Res. 53, S131-S139 (2009). open in new tab
- Böttger, F. et al. Which casein in sodium caseinate is most resistant to in vitro digestion? Effect of emulsification and enzymatic structuring. Food Hydrocoll. 88, 114-118 (2019). open in new tab
- Suh, J., Dawson, M. & Hanes, J. Real-time multiple-particle tracking: Applications to drug and gene delivery. Adv. Drug Deliv. Rev. 57, 63-78 (2005). open in new tab
- Dawson, M., Wirtz, D. & Hanes, J. Enhanced viscoelasticity of human cystic fibrotic sputum correlates with increasing microheterogeneity in particle transport. J. Biol. Chem. 278, 50393-50401 (2003). open in new tab
- Kues, T., Peters, R. & Kubitscheck, U. Visualization and tracking of single protein molecules in the cell nucleus. Biophys. J. 80, 2954-2967 (2001). open in new tab
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