Transport of particles in intestinal mucus under simulated infant and adult physiological conditions: Impact of mucus structure and extracellular DNA

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Macierzanka, Adam ^a,b,c   Mackie, Alan R ^a   Bajka, Balazs H ^a   Rigby, Neil M ^a   Nau, Françoise ^b,c   Dupont, Didier ^b,c  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^b CNRS   (France)

^c CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; MUCIN; DNA;

ABSORPTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD RHEOLOGY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIFFUSION; DIGESTION; DRY WEIGHT; HUMAN; INTESTINE EPITHELIUM; JEJUNUM; MUCUS SECRETION; NONHUMAN; PARTICLE SIZE; PIGLET; SMALL INTESTINE MUCOSA; STOMACH MUCUS; VISCOSITY; AGING; ANIMAL; CYTOLOGY; EXTRACELLULAR SPACE; FLOW KINETICS; INTESTINE MUCOSA; METABOLISM; MUCUS; PHYSIOLOGY; SMALL INTESTINE; STATIC ELECTRICITY; SWINE; TRANSPORT AT THE CELLULAR LEVEL;

AGING; ANIMALS; BIOLOGICAL TRANSPORT; DIFFUSION; DNA; EXTRACELLULAR SPACE; INTESTINAL MUCOSA; INTESTINE, SMALL; MUCUS; RHEOLOGY; STATIC ELECTRICITY; SUS SCROFA; VISCOSITY;

EID: 84899703635     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095274     Document Type: Article

References (44)

1. Johansson MEV, Sjövall H, Hansson GC (2013) The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol 10: 352-361.
2. Cone RA (2009) Barrier properties of mucus. Adv Drug Deliv Rev 61: 75-85.
3. Lindén SK, Florin THJ, McGuckin MA (2008) Mucin dynamics in intestinal bacterial infection. PLoS One 3: e3952. doi:10.1371/journal.pone. 0003952.
4. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA (2008) Mucins in the mucosal barrier to infection. Mucosal Immunol 1: 183-197. (Pubitemid 351541304)
5. Atuma C, Strugala V, Allen A, Holm L (2001) The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol Gastrointest Liver Physiol 280: G922-G929.
6. Crater JS, Carrier RL (2010) Barrier properties of gastrointestinal mucus to nanoparticle transport. Macromol Biosci 10: 1473-1483.
7. Macierzanka A, Rigby NM, Corfield AP, Wellner N, Böttger F, et al. (2011) Adsorption of bile salts to particles allows penetration of intestinal mucus. Soft Matter 7: 8077-8084.
8. Macierzanka A, Böttger F, Rigby NM, Lille M, Poutanen K, et al. (2012) Enzymatically structured emulsions in simulated gastrointestinal environment: Impact on interfacial proteolysis and diffusion in intestinal mucus, Langmuir 28: 17349-17362.
9. Forstner JF, Oliver MG, Sylvester FA (1995) Production, structure, and biologic relevance of gastrointestinal mucins. In: Blaser MJ, Smith PD, Ravdin JI, Greenberg HB, Guerrant RL, editors. Infections of the gastrointestinal tract. New York: Raven Press. 71-88.
10. van der Flier LG, Clevers H (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71: 241-260.
11. Watson AJM, Chu S, Sieck L, Gerasimenko O, Bullen T, et al. (2005) Epithelial barrier function in vivo is sustained despite gaps in epithelial layers. Gastroenterology 129: 902-912. (Pubitemid 41242683)
12. Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C (2012) Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol 8: 36-45.
13. Hall PA, Coates PJ, Ansari B, Hopwood D (1994) Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci 107: 3569-3577.
14. Watson AJ, Chu S, Montrose MH (2003) Apoptosis is a consequence and not a cause of cell shedding from small intestinal villi: Two-photon microscopy studies in the living mouse. Gastroenterology 124: A27.
15. Leedham SJ, Brittan M, McDonald SAC, Wright NA (2005) Intestinal stem cells. J Cell Mol Med 9: 11-24.
16. Moon HW (1971) Epithelial cell migration in the alimentary mucosa of the suckling pig. Proc Soc Exp Biol Med 137: 151-154.
17. Schmidt GH, Winton DJ, Ponder BAJ (1988) Development of the pattern of cell renewal in the crypt-villus unit of chimaeric mouse small intestine. Development 103: 785-790.
18. Matsuo K, Ota H, Akamatsu T, Sugiyama A, Katsuyama T (1997) Histochemistry of the surface mucous gel layer of the human colon. Gut 40: 782-789. (Pubitemid 27305472)
19. Tadros T (2004) Application of rheology for assessment and prediction of the long-term physical stability of emulsions. Adv Colloid Interface Sci 108-109: 227-258.
20. Potten CS, Loeffler M (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110: 1001-1020. (Pubitemid 120009472)
21. Chernick WS, Barbero GJ (1959) Composition of tracheobronchial secretions in cystic fibrosis of the pancreas and bronchectasis. Pediatrics 24: 739-745.
22. Potter J, Mathews LW, Lemm J, Spector S (1960) The composition of pulmonary secretions from patients with and without cystic fibrosis. Am J Dis Child 100: 493-495.
23. Chernick WS, Barbero GJ, Eichel HJ (1961) In vitro evaluation of effect of enzymes on tracheobronchial secretions from patients with cystic fibrosis. Pediatrics 27: 589-596.
24. Shak S, Capon DJ, Hellmiss R, Marsters SA, Baker CL (1990) Recombinant human DNase reduces the viscosity of cystic fibrosis sputum. Proc Natl Acad Sci USA 87: 9188-9192. (Pubitemid 120030590)
25. Zahm J-M, de Bentzmann SG, Deneuville E, Perrot-Minnot C, Dabadie A, et al. (1995) Dose-dependent in vitro effect of recombinant human DNase on rheological and transport properties of cystic fibrosis respiratory mucus. Eur Respir J 8: 381-386.
26. Georgiades P, Pudney PDA, Thornton DJ, Waigh T (2014) Particle tracking microrheology of purified gastrointestinal mucins. Biopolymers 101: 366-377.
27. Rundell JO, Lecce JG (1972) Independence of intestinal epithelial cell turnover from cessation of absorption of macromolecules (closure) in the neonatal mouse, rabbit, hamster and guinea pig. Biol Neonate 20: 51-57.
28. Al-Nafussi AI, Wright NA (1982) Cell kinetics in the mouse small intestine during immediate postnatal life. Virchows Arch B Cell Pathol 40: 51-62. (Pubitemid 12096430)
29. Grey RD (1968) Epithelial cell migration in the intestine of the young mouse. Dev Biol 18: 501-514.
30. Clarke RM, Hardy RN (1971) Histological changes in the small intestine of the young pig and their relation to macromolecular uptake. J Anat 108: 63-77.
31. Wright NA, Irwin M (1982) The kinetics of villus cell populations in the mouse small intestine I. Normal villi: the steady state requirement. Cell Prolif 15: 595-609. (Pubitemid 12006239)
32. Clarke RM (1972) The effect of growth and of fasting on the number of villi and crypts in the small intestine of the albino rats. J Anat 112: 27-33.
33. Deplancke B, Gaskins HR (2001) Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 73(suppl): 1131S-1141S. (Pubitemid 32496957)
34. Turck D, Feste AS, Lifschitz CH (1993) Age and diet affect the composition of porcine colonic mucins. Pediatr Res 33: 564-567. (Pubitemid 23159450)
35. Dunsford BR, Haensly WE, Knabe DA (1991) Effects of diet on acidic and neutral goblet cell populations in the small intestine of early weaned pigs. Am J Vet Res 52: 1743-1746.
36. Hill RR, Cowley HM, Andremont A (1990) Influence of colonizing microflora on the mucin histochemistry of the neonatal mouse colon. Histochem J 22: 102-105. (Pubitemid 20088801)
37. Deplancke B, Hristova KR, Oakley HA, McCracken VJ, Aminov R, et al. (2000) Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract. Appl Environ Microbiol 66: 2166-2174. (Pubitemid 30253747)
38. Brunsgaard G (1997) Morphological characteristics, epithelial cell proliferation, and crypt fission in cecum and colon of growing pigs. Dig Dis Sci 42: 2384-2393.
39. Hansson GC (2012) Role of mucus layers in gut infection and inflammation. Curr Opin Microbiol 15: 57-62.
40. Bourlieu C, Ménard O, Bouzerzour K, Mandalari G, Macierzanka A, et al. (2014) Specificity of infant digestive conditions: some clues for developing relevant in vitro models. Crit Rev Food Sci Nutr 54: 1427-1457.
41. Gustafsson JK, Ermund A, Johansson MEV, Schütte A, Hansson GC, et al. (2012) An ex vivo method for studying mucus formation, properties, and thickness in human colonic biopsies and mouse small and large intestinal explants. Am J Physiol Gastrointest Liver Physiol 302: G430-G438.
42. Suh J, Dawson M, Hanes J (2005) Real-time multiple-particle tracking: applications to drug and gene delivery. Adv Drug Deliv Rev 57: 63-78. (Pubitemid 39424064)
43. Dawson M, Wirtz D, Hanes J (2003) Enhanced viscoelasticity of human cystic fibrotic sputum correlates with increasing microheterogeneity in particle transport. J Biol Chem 278: 50393-50401. (Pubitemid 37548883)
44. Kues T, Peters R, Kubitscheck U (2001) Visualization and tracking of single protein molecules in the cell nucleus. Biophys J 80: 2954-2967. (Pubitemid 32521667)