An exploration of the microrheological environment around the distal ileal villi and proximal colonic mucosa of the possum (Trichosurus vulpecula)

Journal of the Royal Society Interface

Volumn 10, Issue 81, 2013, Pages

  Lim, Y F ^a   Williams, M A K ^b,c   Lentle, R G ^a,b   Janssen, P W M ^a   Mansel, B W ^b,c   Keen, S A J ^b,c   Chambers, P ^b  

^a MASSEY UNIVERSITY   (New Zealand)

^b MASSEY UNIVERSITY   (New Zealand)

^c MACDIARMID INSTITUTE FOR ADVANCED MATERIALS AND NANOTECHNOLOGY   (New Zealand)

Author keywords

Colon; Ileum; Microrheology; Mucosa

Indexed keywords

MASS TRANSFER; POLYSTYRENES;

COLON; DIFFUSIVE MASS TRANSFER; FLUID ENVIRONMENT; ILEUM; INTESTINAL MUCOSA; MICRORHEOLOGY; MUCOSA; NEWTONIAN FLUIDS;

VISCOSITY;

ANIMAL TISSUE; ARTICLE; COLON MUCOSA; EX VIVO STUDY; ILEUM; NONHUMAN; PARTICLE SIZE; TRICHOSURUS; TRICHOSURUS VULPECULA; VISCOSITY; ANIMAL; COLON; CYTOLOGY; FLOW KINETICS; FLUORESCENCE; HISTOLOGY; IN VITRO STUDY; METHODOLOGY; MICROVILLUS; PHYSIOLOGY; ULTRASTRUCTURE; VIDEO MICROSCOPY;

MICROSPHERE; POLYSTYRENE DERIVATIVE;

ANIMALS; COLON; FLUORESCENCE; ILEUM; MICROSCOPY, VIDEO; MICROSPHERES; MICROVILLI; POLYSTYRENES; RHEOLOGY; TRICHOSURUS; VISCOSITY;

MLCS; MLOWN;

EID: 84875712220     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2012.1008     Document Type: Article

References (58)

1. Read NW, Levin RJ, Holdsworth CD. 1976 Proceedings: Measurement of the functional unstirred layer thickness in the human jejunum in vivo. Gut 17, 387.
2. Westergaard H, Dietschy JM. 1974 Delineation of the dimensions and permeability characteristics of the two major diffusion barriers to passive mucosal uptake in the rabbit intestine. J. Clin. Invest. 54, 718-732. (doi:10.1172/JCI107810)
3. Wilson FA, Sallee VL, Dietschy JM. 1971 Unstirred water layers in intestine: rate determinant of fatty acid absorption from micellar solutions. Science 174, 1031-1033. (doi:10.1126/science.174.4013.1031)
4. Anderson BW, Levine AS, Levitt DG, Kneip JM, Levitt MD. 1988 Physiological measurement of luminal stirring in perfused rat jejunum. Am. J. Physiol. 254, G843-G848.
5. Amidon GL, Kou J, Elliott RL, Lightfoot EN. 1980 Analysis of models for determining intestinal wall permeabilities. J. Pharm. Sci. 69, 1369-1373. (doi:10.1002/jps.2600691204)
6. Levitt MD, Aufderheide T, Fetzer CA, Bond JH, Levitt DG. 1984 Use of carbon monoxide to measure luminal stirring in the rat gut. J. Clin. Invest. 74, 2056-2064. (doi:10.1172/JCI111629)
7. Winne D. 1981 Unstirred layer as a diffusion barrier in vitro and in vivo. In Intestinal absorption and secretion (eds F Skadhause, K Heintse), pp. 21-38. Lancaster, UK: MTP Press.
8. Thomson AB, Dietschy JM. 1977 Derivation of the equations that describe the effects of unstirred water layers on the kinetic parameters of active transport processes in the intestine. J. Theor. Biol. 64, 277-294. (doi:10.1016/0022-5193(77)90357-5)
9. Thomson ABR, Dietschy JM. 1984 The role of the unstirred water layer in intestinal permeation. In Pharmacology of intestinal permeation (ed. TZ Csaky), pp. 165-269. New York, NY: Springer.
10. Debnam ES, Levin RJ. 1975 Effects of fasting and semi-starvation on the kinetics of active and passive sugar absorption across the small intestine in vivo. J. Physiol. 252, 681-700.
11. Winne D. 1978 Dependence of intestinal absorption in vivo on the unstirred layer. Naunyn. Schmiedebergs Arch. Pharmacol. 304, 175-181. (doi:10.1007/BF00495554)
12. Winne D, Kopf S, Ulmer ML. 1979 Role of unstirred layer in intestinal absorption of phenylalanine in vivo. Biochim. Biophys. Acta 550, 120-130. (doi:10. 1016/0005-2736(79)90120-2)
13. Fagerholm U, Lennernäs H. 1995 Experimental estimation of the effective unstirred water layer thickness in the human jejunum, and its importance in oral drug absorption. Eur. J. Pharm. Sci. 3, 247-253. (doi:10.1016/0928-0987(95)00027-B)
14. Pohl P, Saparov SM, Antonenko YN. 1998 The size of the unstirred layer as a function of the solute diffusion coefficient. Biophys. J. 75, 1403-1409. (doi:10.1016/S0006-3495(98)74058-5)
15. Sellers LA, Allen A, Morris ER, Ross-Murphy SB. 1991 The rheology of pig small intestinal and colonic mucus: weakening of gel structure by non-mucin components. Biochim. Biophys. Acta 1115, 174-179. (doi:10.1016/0304-4165(91) 90027-E)
16. Smithson KW, Millar DB, Jacobs LR, Gray GM. 1981 Intestinal diffusion barrier: unstirred water layer or membrane surface mucous coat? Science 214, 1241-1244. (doi:10.1126/science.7302593)
17. Szentkuti L, Lorenz K. 1995 The thickness of the mucus layer in different segments of the rat intestine. Histochem. J. 27, 466-472.
18. Atuma C, Strugala V, Allen A, Holm L. 2001 The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am. J. Physiol. 280, G922-G929.
19. Sugano K. 2009 Estimation of effective intestinal membrane permeability considering bile micelle solubilisation. Int. J. Pharm. 368, 116-122. (doi:10. 1016/j.ijpharm.2008.10.001)
20. 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. (doi:10.1016/j.addr.2004.06.001)
21. Swidsinski A, Loening-Baucke V, Theissig F, Engelhardt H, Bengmark S, Koch S, Lochs H, Doerffel Y. 2007 Comparative study of the intestinal mucus barrier in normal and inflamed colon. Gut 56, 343-350. (doi:10.1136/gut.2006. 098160)
22. Danielsen EM, Sjöström H, Norén O, Bro B, Dabelsteen E. 1982 Biosynthesis of intestinal microvillar proteins. Characterization of intestinal explants in organ culture and evidence for the existence of pro-forms of the microvillar enzymes. Biochem. J. 202, 647-654.
23. Ham AW. 1974 Histology, 7th edn. Philadelphia: Lippincott.
24. Weinstein LD, Shoemaker CP, Hersh T, Wright HK. 1969 Enhanced intestinal absorption after small bowel resection in man. Arch. Surg. 99, 560-562. (doi:10.1001/archsurg.1969.01340170012003)
25. Lentle RG, Hemar Y, Hall CE, Stafford KJ. 2005 Periodic fluid extrusion and models of digesta mixing in the intestine of a herbivore, the common brushtail possum (Trichosurus vulpecula). J. Comp. Physiol. B175, 337-347.
26. MacKintosh FC, Schmidt CF. 1999 Microrheology. Curr. Opin. Colloid. Interface Sci. 4, 300-307. (doi:10.1016/S1359-0294(99)90010-9)
27. Macierzanka A, Rigby NM, Corfield AP, Wellner N, Böttger F, Mills ENC, Mackie AR. 2011 Adsorption of bile salts to particles allows penetration of intestinal mucus. Soft Matter 7, 8077-8084. (doi:10.1039/c1sm05888f)
28. 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, 50 393-50 401 (doi:10.1074/jbc.M309026200)
29. Crater JS, Carrier RL. 2010 Barrier properties of gastrointestinal mucus to nanoparticle transport. Macromol. Biosci. 10, 1473-1483. (doi:10.1002/mabi. 201000137)
30. Rogers SS, Waigh TA, Zhao X, Lu Jr. 2007 Precise particle tracking against a complicated background: polynomial fitting with Gaussian weight. Phys. Biol. 4, 220-227. (doi:10.1088/1478-3975/4/3/008)
31. Gardel ML, Valentine MT, Weitz DA. 2005 Microrheology. In Microscale diagnostic techniques (ed. KS Breuer), pp. 1-50. Berlin, Germany: Springer.
32. Waigh TA. 2005 Microrheology of complex fluids. Rep. Prog. Phys. 68, 685-742. (doi:10.1088/0034-4885/68/3/R04)
33. Mason TG. 2000 Estimating the viscoelastic moduli of complex fluids using the generalized Stokes-Einstein equation. Rheol. Acta 39, 371-378. (doi:10.1007/s003970000094)
34. Lentle RG, Janssen PWM. 2011 Flow, mixing and absorption at the mucosa. In Physical processes of digestion (eds RG Lentle, PWM Janssen), pp. 234-294. New York, NY: Springer.
35. Taylor C, Allen A, Dettmar PW, Pearson JP. 2003 The gel matrix of gastric mucus is maintained by a complex interplay of transient and nontransient associations. Biomacromolecules 4, 922-927. (doi:10.1021/bm025767t)
36. Valentine MT, Kaplan PD, Thota D, Crocker JC, Gisler T, Prud'homme RK, Beck M, Weitz DA. 2001 Investigating the microenvironments of inhomogeneous soft materials with multiple particle tracking. Phys. Rev. E 64, 1-9.
37. Lai SK, O'Hanlon DE, Harrold S, Man ST, Wang YY, Cone R, Hanes J. 2007 Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus. Proc. Natl Acad. Sci. USA 104, 1482-1487. (doi:10.1073/pnas.0608611104)
38. Olmsted SS, Padgett JL, Yudin AI, Whaley KJ, Moench TR, Cone RA. 2001 Diffusion of macromolecules and virus-like particles in human cervical mucus. Biophys. J. 81, 1930-1937. (doi:10.1016/S0006-3495(01)75844-4)
39. Williams MAK, Vincent RR, Pinder DN, Hemar Y. 2008 Microrheological studies offer insights into polysaccharide gels. J. Non-Newtonian Fluid Mech. 149, 63-70. (doi:10.1016/j.jnnfm.2007.05.006)
40. de Gennes PG. 1971 Reptation of a polymer chain in the presence of fixed obstacles. J. Chem. Phys. 55, 572-579. (doi:10.1063/1.1675789)
41. Cone RA. 2009 Barrier properties of mucus. Adv. Drug Deliv. Rev. 61, 75-85. (doi:10.1016/j.addr. 2008.09.008)
42. Sawaguchi A, Ishihara K, Kawano J, Oinuma T, Hotta K, Suganuma T. 2002 Fluid dynamics of the excretory flow of zymogenic and mucin contents in rat gastric gland processed by high-pressure freezing/freeze substitution. J. Histochem. Cytochem. 50, 223-234. (doi:10.1177/002215540205000210)
43. 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. (doi:10.1136/gut.40.6.782)
44. Swidsinski A, Sydora BC, Doerffel Y, Loening-Baucke V, Vaneechoutte M, Lupicki M, Scholze J, Lochs H, Dieleman LA. 2007 Viscosity gradient within the mucus layer determines the mucosal barrier function and the spatial organization of the intestinal microbiota. Inflamm. Bowel Dis. 13, 963-970. (doi:10.1002/ibd.20163)
45. Verdugo P. 1990 Goblet cells secretion and mucogenesis. Annu. Rev. Physiol. 52, 157-176. (doi:10.1146/annurev.ph.52.030190.001105)
46. Whitaker M, Zimmerberg J. 1987 Inhibition of secretory granule discharge during exocytosis in sea urchin eggs by polymer solutions. J. Physiol. 389, 527-539.
47. Chandler DE, Whitaker M, Zimmerberg J. 1989 High molecular weight polymers block cortical granule exocytosis in sea urchin eggs at the level of granule matrix disassembly. J. Cell Biol. 109, 1269-1278. (doi:10.1083/jcb.109. 3.1269)
48. Verdugo P. 1993 Polymer gel phase transition in condensation- decondensation of secretory products. Adv. Polym. Sci. 110, 145-156. (doi:10.1007/BFb0021131)
49. Jeffery PK, Li D. 1997 Airway mucosa: secretory cells, mucus and mucin genes. Eur. Respir. J. 10, 1655-1662. (doi:10.1183/09031936.97.10071655)
50. Davis CW, Dowell ML, Lethem M, Van Scott M. 1992 Goblet cell degranulation in isolated canine tracheal epithelium: response to exogenous ATP, ADP, and adenosine. Am. J. Physiol. 262, C1313-C1323.
51. Lethem M, Dowell M, Van Scott M, Yankaskas J, Egan T, Boucher R, Davis C. 1993 Nucleotide regulation of goblet cells in human airway epithelial explants: normal exocytosis in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 9, 315.
52. McConnell RE, Higginbotham JN, Shifrin Jr DA, Tabb DL, Coffey RJ, Tyska MJ. 2009 The enterocyte microvillus is a vesicle-generating organelle. J. Cell Biol. 185, 1285-1298. (doi:10.1083/jcb.200902147)
53. Dawson M, Krauland E, Wirtz D, Hanes J. 2004 Transport of polymeric nanoparticle gene carriers in gastric mucus. Biotechnol. Prog. 20, 851-857. (doi:10.1021/bp0342553)
54. Lentle RG, De Loubens C, Hulls C, Janssen PWM, Golding MD, Chambers JD. 2012 Organization of longitudinal and circular contractions during pendular and segmental activity; a comparison of duodenal contractile activity in the rat and guinea pig. Neurogastroenterol. Mot. 24, 686-695, e298. (doi:10.1111/j.1365- 2982.2012.01923.x)
55. Grivel ML, Ruckebusch Y. 1972 The propagation of segmental contractions along the small intestine. J. Physiol. 227, 611-625.
56. Robbe C, Capon C, Maes E, Rousset M, Zweibaum A, Zanetta JP, Michalski JC. 2003 Evidence of regiospecific glycosylation in human intestinal mucins. J. Biol. Chem. 278, 46 337-46 348. (doi:10.1074/jbc.M302529200)
57. Kararli TT. 1995 Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm. Drug Dispos. 16, 351-380. (doi:10.1002/bdd. 2510160502)
58. Boshi Y et al. 1996 Developmental changes in distribution of the mucous gel layer and intestinal permeability in rat small intestine. J. Parenter. Enteral Nutr. 20, 406-411. (doi:10.1177/0148607196020006406)