Elucidating the signaling mechanism of an epithelial tight-junction opening induced by chitosan

Biomaterials

Volumn 33, Issue 26, 2012, Pages 6254-6263

  Hsu, Li Wen ^a   Lee, Pei Ling ^a   Chen, Chiung Tong ^b   Mi, Fwu Long ^c   Juang, Jyuhn Huarng ^d   Hwang, Shiaw Min ^e   Ho, Yi Cheng ^c   Sung, Hsing Wen ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^c VANUNG UNIVERSITY   (Taiwan)

^d CHANG GUNG UNIVERSITY   (Taiwan)

^e FOOD INDUSTRY RESEARCH AND DEVELOPMENT INSTITUTE   (Taiwan)

Author keywords

Chitosan; Integrin receptor; Oral drug delivery; Paracellular permeability; Tyrosine kinase

Indexed keywords

CACO-2 CELLS; CYTOSOLS; EPITHELIAL CELLS; HYDROPHILIC MACROMOLECULES; INTEGRIN RECEPTORS; INTEGRINS; INTESTINAL CELLS; ORAL DRUG DELIVERY; PARACELLULAR PERMEABILITY; PERMEATION ENHANCERS; SIGNALING MECHANISMS; TIGHT JUNCTIONS; TYROSINE KINASE;

AMINO ACIDS; BIOCHEMISTRY; CELL MEMBRANES; CYTOLOGY; DRUG DELIVERY; ENZYMES; MONOLAYERS; PHOSPHORYLATION;

CHITOSAN;

CELL SURFACE PROTEIN; CHITOSAN; FOCAL ADHESION KINASE; INTEGRIN RECEPTOR; VITRONECTIN RECEPTOR;

ARTICLE; BIOAVAILABILITY; CELL ADHESION; CELL MEMBRANE; CELL STRAIN CACO 2; CONTROLLED STUDY; CYTOSOL; DOWN REGULATION; EPITHELIUM CELL; MACROMOLECULE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SIMULATION; TIGHT JUNCTION;

BLOTTING, WESTERN; CACO-2 CELLS; CELL MEMBRANE; CHITOSAN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MODELS, BIOLOGICAL; MOLECULAR DYNAMICS SIMULATION; PROTEIN-TYROSINE KINASES; TIGHT JUNCTIONS;

EID: 84862842747     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.05.013     Document Type: Article

References (52)

1. Su F.Y., Lin K.J., Sonaje K., Wey S.P., Yen T.C., Ho Y.C., et al. Protease inhibition and absorption enhancement by functional nanoparticles for effective oral insulin delivery. Biomaterials 2012, 33:2801-2811.
2. Chen M.C., Sonaje K., Chen K.J., Sung H.W. A review of the prospects for polymeric nanoparticle platforms in oral insulin delivery. Biomaterials 2011, 32:9826-9838.
3. Tsukita S., Furuse M., Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001, 2:285-293.
4. Thanou M., Verhoef J.C., Junginger H.E. Chitosan and its derivatives as intestinal absorption enhancers. Adv Drug Deliv Rev 2001, 50:S91-S101.
5. Thanou M., Verhoef J.C., Junginger H.E. Oral drug absorption enhancement by chitosan and its derivatives. Adv Drug Deliv Rev 2001, 52:117-126.
6. Kotzé A.F., Luessen H.L., de Leeuw B.J., de Boer A.G., Verhoef J.C., Junginger H.E. Comparison of the effect of different chitosan salts and N-trimethyl chitosan chloride on the permeability of intestinal epithelial cells (Caco-2). J Control Release 1998, 51:35-46.
7. Chen M.C., Mi F.L., Liao Z.X., Sung H.W. Chitosan: its applications in drug eluting devices. Adv Polym Sci 2011, 243:185-230.
8. Mhurchu C.N., Poppitt S.D., McGill A.T., Leahy F.E., Bennett D.A., Lin R.B., et al. The effect of the dietary supplement, chitosan, on body weight: a randomised controlled trial in 250 overweight and obese adults. Int J Obes Relat Metab Disord 2004, 28:1149-1156.
9. Chen M.C., Wong H.S., Lin K.J., Chen H.L., Wey S.P., Sonaje K., et al. The characteristics, biodistribution and bioavailability of a chitosan-based nanoparticulate system for the oral delivery of heparin. Biomaterials 2009, 30:6629-6637.
10. Sonaje K., Chen Y.J., Chen H.L., Wey S.P., Juang J.H., Nguyen H.N., et al. Enteric-coated capsules filled with freeze-dried chitosan/poly(gamma-glutamic acid) nanoparticles for oral insulin delivery. Biomaterials 2010, 31:3384-3394.
11. 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 Deliv Rev 2005, 57:1583-1594.
12. Artursson P., Lindmark T., Davis S.S., Illum L. Effect of chitosan on the permeability of monolayers of intestinal epithelial cells (Caco-2). Pharm Res 1994, 11:1358-1361.
13. Smith J.M., Dornish M., Wood E.J. Involvement of protein kinase C in chitosan glutamate-mediated tight junction disruption. Biomaterials 2005, 26:3269-3276.
14. Sonaje K., Lin Y.H., Juang J.H., Wey S.P., Chen C.T., Sung H.W. In vivo evaluation of safety and efficacy of self-assembled nanoparticles for oral insulin delivery. Biomaterials 2009, 30:2329-2339.
15. Rosenthal R., Günzel D., Finger C., Krug S.M., Richter J.F., Schulzke J.D., et al. The effect of chitosan on transcellular and paracellular mechanisms in the intestinal epithelial barrier. Biomaterials 2012, 33:2791-2800.
16. Balda M.S., Matter K. Tight junctions at a glance. J Cell Sci 2008, 121:3677-3682.
17. Matter K., Balda M.S. Signalling to and from tight junctions. Nat Rev Mol Cell Biol 2003, 4:225-236.
18. Tsukita S., Furuse M. Pores in the wall: claudins constitute tight junction strands containing aqueous pores. J Cell Biol 2000, 149:13-16.
19. Heiskala M., Peterson P.A., Yang Y. The roles of claudin superfamily proteins in paracellular transport. Traffic 2001, 2:93-98.
20. Meyer T.N., Schwesinger C., Ye J., Denker B.M., Nigam S.K. Reassembly of the tight junction after oxidative stress depends on tyrosine kinase activity. J Biol Chem 2001, 276:22048-22055.
21. Staddon J.M., Herrenknecht K., Smales C., Rubin L.L. Evidence that tyrosine phosphorylation may increase tight junction permeability. J Cell Sci 1995, 108:609-619.
22. Yeh T.H., Hsu L.W., Tseng M.T., Lee P.L., Sonjae K., Ho Y.C., et al. Mechanism and consequence of chitosan-mediated reversible epithelial tight junction opening. Biomaterials 2011, 32:6164-6173.
23. Szolnoky G., Bata-Csörgö Z., Kenderessy A.S., Kiss M., Pivarcsi A., Novák Z., et al. A mannose-binding receptor is expressed on human keratinocytes and mediates killing of Candida albicans. J Invest Dermatol 2001, 117:205-213.
24. Mujumdar R.B., Ernst L.A., Mujumdar S.R., Lewis C.J., Waggoner A.S. Cyanine dye labeling reagents: sulfoindocyanine succinimidyl esters. Bioconjug Chem 1993, 4:105-111.
25. Hayner N.T., Driscoll J., Ferayorni L., Spies-Karotkin G., Jauregui H.O. Ponceaus S: a sensitive method for protein determination in freshly isolated and cultured cells. J Tissue Cult Methods 1982, 7:77-80.
26. Sun H., Chow E.C., Liu S., Du Y., Pang K.S. The Caco-2 cell monolayer: usefulness and limitations. Expert Opin Drug Metab Toxicol 2008, 4:395-411.
27. Keely S., Rullay A., Wilson C., Carmichael A., Carrington S., Corfield A., et al. In vitro and ex vivo intestinal tissue models to measure mucoadhesion of poly (methacrylate) and N-trimethylated chitosan polymers. Pharm Res 2005, 22:38-49.
28. Dhaliwal S., Jain S., Singh H.P., Tiwary A.K. Mucoadhesive microspheres for gastroretentive delivery of acyclovir: in vitro and in vivo evaluation. AAPS J 2008, 10:322-330.
29. Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., et al. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 1987, 262:5592-5595.
30. Wells C.L., Jechorek R.P., Kinneberg K.M., Debol S.M., Erlandsen S.L. The isoflavone genistein inhibits internalization of enteric bacteria by cultured Caco-2 and HT-29 enterocytes. J Nutr 1999, 129:634-640.
31. Volberg T., Zick Y., Dror R., Sabanay I., Gilon C., Levitzki A., et al. The effect of tyrosine-specific protein phosphorylation on the assembly of adherens-type junctions. EMBO J 1992, 11:1733-1742.
32. Sheth P., Delos Santos N., Seth A., LaRusso N.F., Rao R.K. Lipopolysaccharide disrupts tight junctions in cholangiocyte monolayers by a c-Src-, TLR4-, and LBP-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 2007, 293. G308-18.
33. Zhang Q., Thomas S.M., Lui V.W., Xi S., Siegfried J.M., Fan H., et al. Phosphorylation of TNF-alpha converting enzyme by gastrin-releasing peptide induces amphiregulin release and EGF receptor activation. Proc Natl Acad Sci USA 2006, 103:6901-6906.
34. Lechner A.M., Assfalg-Machleidt I., Zahler S., Stoeckelhuber M., Machleidt W., Jochum M., et al. RGD-dependent binding of procathepsin X to integrin alphavbeta3 mediates cell-adhesive properties. J Biol Chem 2006, 281:39588-39597.
35. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
36. Wang C., Prossnitz E.R., Roy S.K. Expression of G protein-coupled receptor 30 in the hamster ovary: differential regulation by gonadotropins and steroid hormones. Endocrinology 2007, 148:4853-4864.
37. Peng S.F., Tseng M.T., Ho Y.C., Wei M.C., Liao Z.X., Sung H.W. Mechanisms of cellular uptake and intracellular trafficking with chitosan/DNA/poly (gamma-glutamic acid) complexes as a gene delivery vector. Biomaterials 2011, 32:239-248.
38. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., et al. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 2004, 25:1605-1612.
39. Eyster K.M. Introduction to signal transduction: a primer for untangling the web of intracellular messengers. Biochem Pharmacol 1998, 55:1927-1938.
40. Bueno L., Fioramonti J. Protease-activated receptor 2 and gut permeability: a review. Neurogastroenterol Motil 2008, 20:580-587.
41. Hamilton J.R., Chow J.M., Cocks T.M. Protease-activated receptor-2 turnover stimulated independently of receptor activation in porcine coronary endothelial cells. Br J Pharmacol 1999, 127:617-622.
42. Lin Y.H., Mi F.L., Chen C.T., Chang W.C., Peng S.F., Liang H.F., et al. Preparation and characterization of nanoparticles shelled with chitosan for oral insulin delivery. Biomacromolecules 2007, 8:146-152.
43. Sonaje K., Chuang E.Y., Lin K.J., Yen T.C., Su F.Y., Tseng M.T., et al. Opening of epithelial tight junctions and enhancement of paracellular permeation by chitosan: microscopic, ultra-structural and computed-tomographic observations. Mol Pharm 2012, 9:1271-1279.
44. Ranaldi G., Marigliano I., Vespignani I., Perozzi G., Sambuy Y. The effect of chitosan and other polycations on tight junction permeability in the human intestinal Caco-2 cell line. J Nutr Biochem 2002, 13:157-167.
45. Quintela-Fandino M., González-Martín A., Colomer R. Targeting cytoskeleton reorganisation as antimetastatic treatment. Clin Transl Oncol 2010, 12:662-669.
46. Gilcrease M.Z. Integrin signaling in epithelial cells. Cancer Lett 2007, 247:1-25.
47. Alghisi G.C., Ponsonnet L., Rüegg C. The integrin antagonist cilengitide activates alphaVbeta3, disrupts VE-cadherin localization at cell junctions and enhances permeability in endothelial cells. PLoS One 2009, 4:e4449.
48. Legate K.R., Wickström S.A., Fässler R. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 2009, 23:397-418.
49. Kozlova N.I., Morozevich G.E., Chubukina A.N., Berman A.E. Integrin alphaVbeta3 promotes anchorage-dependent apoptosis in human intestinal carcinoma cells. Oncogene 2001, 20:4710-4717.
50. Xiong J.P., Stehle T., Diefenbach B., Zhang R., Dunker R., Scott D.L., et al. Crystal structure of the extracellular segment of integrin alphaVbeta3. Science 2001, 294:339-345.
51. Rinaudo M. Chitin and chitosan: properties and applications. Prog Polym Sci 2006, 31:603-632.
52. Triantafilou M., Triantafilou K., Wilson K.M. A 70 kDa MHC class I associated protein (MAP-70) identified as a receptor molecule for Coxsackievirus A9 cell attachment. Hum Immunol 2000, 61:867-878.