Intracellular mechanisms involved in docosahexaenoic acid-induced increases in tight junction permeability in Caco-2 cell monolayers

Journal of Nutrition

Volumn 140, Issue 9, 2010, Pages 1557-1563

  Roig Pérez, Sònia ^a   Cortadellas, Núria ^a   Moretó, Miquel ^a   Ferrer, Ruth ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

1 (5 IODONAPHTALENE 1 SULFONYL) 1H HEXAHYDRO 1,4 DIAZEPINE HYDROCHLORIDE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; AA 961; CALCIMYCIN; CALCIUM ION; CHELERYTHRINE; CHLORIDE; DOCOSAHEXAENOIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; INDOMETACIN; LIPOXYGENASE; LIPOXYGENASE INHIBITOR; MANNITOL; MYOSIN LIGHT CHAIN KINASE INHIBITOR; OCCLUDIN; PHOSPHOLIPASE C; PROSTAGLANDIN SYNTHASE; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN CACO 2; CONTROLLED STUDY; ELECTRIC RESISTANCE; IMMUNOGOLD STAINING; INTRACELLULAR SIGNALING; MEMBRANE PERMEABILITY; SIGNAL TRANSDUCTION; TIGHT JUNCTION;

BENZOQUINONES; CACO-2 CELLS; CALCIUM; CYCLOOXYGENASE INHIBITORS; DOCOSAHEXAENOIC ACIDS; HUMANS; INDOMETHACIN; LIPOXYGENASE INHIBITORS; PERMEABILITY; PROTEIN KINASE C; TIGHT JUNCTIONS; TYPE C PHOSPHOLIPASES;

EID: 77956573976     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.109.120469     Document Type: Article

References (53)

1. Horrocks LA, Yeo YK. Health benefits of docosahexaenoic acid (DHA). Pharmacol Res. 1999;40:211-25.
2. Naito Y, Yoshikawa T. Oxidative stress involvement and gene expression in indomethacin-induced gastropathy. Redox Rep. 2006;11: 243-53. (Pubitemid 46062349)
3. Kaplan M, Mutlu EA, Benson M, Fields JZ, Banan A, Keshawarzian A. Use of herbal preparations in the treatment of oxidant-mediated inflammatory disorders. Complement Ther Med. 2007;15:207-16. (Pubitemid 47250488)
4. Roig-Pérez S, Guardiola F, Moretó M, Ferrer R. Lipid peroxidation induced by docosahexaenoic acid-enrichment modifies paracellular permeability in Caco-2 cells: protective role of taurine. J Lipid Res. 2004;45:1418-28. (Pubitemid 39006969)
5. Roig-Pérez S, Ferrer C, Rafecas M, Moretó M, Ferrer R. Correlation of taurine transport with membrane lipid composition and peroxidation in DHA-enriched Caco-2 cells. J Membr Biol. 2009;228:141-50.
6. Alexander JW. Immunonutrition: the role of omega-3 fatty acids. Nutrition. 1998;14:627-33.
7. Shin K, Fogg VC, Margolis B. Tight junctions and cell polarity. Annu Rev Cell Dev Biol. 2006;22:207-35.
8. Usami M, Muraki K, Iwamoto M, Ohata A, Matsushita E, Miki A. Effect of eicosapentanoic acid (EPA) on tight junction permeability in intestinal monolayer cells. Clin Nutr. 2001;20:351-9. (Pubitemid 32785477)
9. Roche HM, Terres AM, Black IB, Gibney MJ, Kelleher D. Fatty acids and epithelial permeability: effect of conjugated linoleic acid in Caco-2 cells. Gut. 2001;48:797-802. (Pubitemid 32476981)
10. Padma M, Das UN. Effect of cis-unsaturated fatty acids on the activity of protein kinases and protein phosphorylation in macrophage tumor (AK-5) cells in vitro. Prostaglandins Leukot Essent Fatty Acids. 1999; 60:55-63. (Pubitemid 29182166)
11. i via inositol 1,4,5-triphosphate production and activates protein kinase C-gamma and -delta via phosphatidylserine binding site: implication in apoptosis in U937 cells. Mol Pharmacol. 2007;72:1545-56.
12. Gonzalez-Mariscal L, Tapia R, Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim Biophys Acta. 2008; 1778:729-56. (Pubitemid 351317800)
13. Spurr AR. A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res. 1969;26:31-43.
14. Reynolds ES. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963;17:208-12.
15. Seligman AM, Wasserkrug HL, Hanker JS. A new staining method (OTO) for enhancing contrast of lipid-containing membranes and droplets in osmium tetroxide-fixed tissue with osmiophilic thiocarbohydrazide (TCH). J Cell Biol. 1966;30:424-32.
16. Tokuyasu KT. Use of poly(vinylpyrrolidone) and poly(vinyl alcohol) for cryoultramicrotomy. Histochem J. 1989;21:163-71.
17. Awad AB, Young AL, Fink CS. The effect of unsaturated fatty acids on membrane composition and signal transduction in HT-29 human colon cancer cells. Cancer Lett. 1996;108:25-33.
18. Lindmark T, Kimura Y, Artursson P. Absorption enhancement through intracellular regulation of tight junction permeability by medium chain fatty acids in Caco-2 cells. J Pharmacol Exp Ther. 1998;284: 362-9. (Pubitemid 28109567)
19. Matter K, Balda MS. Signalling to and from tight junctions. Nat Rev Mol Cell Biol. 2003;4:225-36.
20. González-Mariscal L, Chávez de Ramírez B, Cereijido M. Tight junction formation in cultured epithelial cells (MDCK). J Membr Biol. 1985;86:113-25. (Pubitemid 15043232)
21. Stuart RO, Sun A, Panichas M, Hebert SC, Brenner BM, Nigam SK. Critical role for intracellular calcium in tight junction biogenesis. J Cell Physiol. 1994;159:423-33. (Pubitemid 24188982)
22. Cereijido M, Contreras RG, Shoshani L, Flores-Benitez D, Larre I. Tight junction and polarity interaction in the transporting epithelial phenotype. Biochim Biophys Acta. 2008;1778:770-93. (Pubitemid 351317802)
23. Ma TY, Tran D, Hoa N, Nguyen D, Merryfield M, Tarnawski A. Mechanism of extracellular calcium regulation of intestinal epithelial tight junction permeability: role of cytoskeletal involvement. Microsc Res Tech. 2000;51:156-68.
24. Seth A, Sheth P, Elias BC, Rao R. Protein phosphatases 2A and 1 interact with occludin and negatively regulate the assembly of tight junctions in the Caco-2 cell monolayer. J Biol Chem. 2007;282: 11487-98. (Pubitemid 47100808)
25. Martinez-Palomo A, Meza I, Beaty G, Cereijido M. Experimental modulation of occludin junctions in a cultured transporting epithelium. J Cell Biol. 1980;87:736-45. (Pubitemid 11161805)
26. 51Cr release. Pharmacology. 1991;42:156-68.
27. 2+: a protein kinase C effect. JMembr Biol. 1996;149: 71-9.
28. 2+ pool in T cells through a mechanism independent of phosphoinositide turnover. J Biol Chem. 1990;265:902-7.
29. Palakurthi SS, Flückiger R, Aktas H, Changolkar AK, Shahsafaei A, Harneit S, Kilic E, Halperin JA. Inhibition of translation initiation mediates the anticancer effect of the n-3 polyunsaturated fatty acid eicosapentaenoic acid. Cancer Res. 2000;60:2919-25. (Pubitemid 30395816)
30. Aktas H, Halperin JA. Translational regulation of gene expression by omega-3 fatty acids. J Nutr. 2004;134:S2487-91.
31. i levels in acutely isolated mouse thymocytes. Cell Biochem Funct. 2009;27: 155-61.
32. Andreeva AY, Piontek J, Blasig IE, Utepbergenov DI. Assembly of tight junction is regulated by the antagonism of conventional and novel protein kinase C isoforms. Int J Biochem Cell Biol. 2006;38: 222-33. (Pubitemid 41619451)
33. Ebner HL, Fiechtner B, Pelster B, Krumschnabel G. Extracellular signal regulated MAP-kinase signalling in osmotically stressed trout hepatocytes. Biochim Biophys Acta. 2006;1760:941-50. (Pubitemid 43816184)
34. Speizer LA, Watson MJ, Brunton LL. Differential effects of omega-3 fish oils on protein kinase activities in vitro. Am J Physiol. 1991;261: E109-14.
35. Huang ZH, Hii CS, Rathjen DA, Poulos A, Murray AW, Ferrante A. N-6 and n-3 polyunsaturated fatty acids stimulate translocation of protein kinase Cα, -βI, -βII and -ε and enhance agonist-induced NADPH oxidase in macrophages. Biochem J. 1997;325:553-7. (Pubitemid 27338740)
36. Sung M, Kim I, Park M, Whang U, Lee M. Differential effects of dietary fatty acids on the regulation of CYP2E1 and protein kinase C in human hepatoma HepG2 cells. J Med Food. 2004;7:197-203. (Pubitemid 38891075)
37. Farhadi A, Keshavarzian A, Ranjbaran Z, Fields JZ, Banan A. The role of protein kinase C isoforms in modulating injury and repair of the intestinal barrier. J Pharmacol Exp Ther. 2006;316:1-7. (Pubitemid 41832574)
38. Farber JL. Mechanisms of cell injury by activated oxygen species. Environ Health Perspect. 1994;102:17-24.
39. Gopalakrishna R, Jaken S. Protein kinase C signaling and oxidative stress. Free Radic Biol Med. 2000;28:1349-61. (Pubitemid 30621479)
40. 2+ through two distinct mechanisms in rat hepatocytes. Acta Pharmacol Sin. 2009;30:78-89.
41. Rao RK, Basuroy S, Rao VU, Karnaky KJ, Gupta A. Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress. Biochem J. 2002; 368:471-81. (Pubitemid 35454525)
42. Martín-Venegas R, Roig-Pérez S, Ferrer R, Moreno JJ. Arachidonic acid cascade and epithelial barrier function during Caco-2 cell differentiation. J Lipid Res. 2006;47:1416-23. (Pubitemid 44079895)
43. Simopoulos AP. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother. 2002;56:365-79.
44. Burke A, Lichtenstein GR, Rombeau JL. Nutrition and ulcerative colitis. Baillieres Clin Gastroenterol. 1997;11:153-74.
45. Chen Q, Nilsson A. Desaturation and chain elongation of n-3 and n-6 polyunsaturated fatty acids in the human CaCo-2 cell line. Biochim Biophys Acta. 1993;1166:193-201.
46. Usami M, Komurasaki T, Hanada A, Kinoshita K, Ohata A. Effect of gamma-linolenic acid or docosahexaenoic acid on tight junction permeability in intestinal monolayer cells and their mechanism by protein kinase C activation and/or eicosanoid formation. Nutrition. 2003;19: 150-6.
47. Balda MS, Matter K. Tight junctions. J Cell Sci. 1998;111:541-7.
48. Balda MS, Gonzalez-Mariscal L, Matter K, Cereijido M, Anderson JM. Assembly of the tight junction: the role of diacylglycerol. J Cell Biol. 1993;123:293-302. (Pubitemid 23313955)
49. Andreeva AY, Krause E, Müller EC, Blasig IE, Utepbergenov DI. Protein kinase C regulates the phosphorylation and cellular localization of occludin. J Biol Chem. 2001;276:38480-6. (Pubitemid 37371200)
50. Farshori P, Kachar B. Redistribution and phosphorylation of occludin during opening and resealing of tight junctions in cultured epithelial cells. J Membr Biol. 1999;170:147-56. (Pubitemid 29367693)
51. Clarke H, Soler AP, Mullin JM. Protein kinase C activation leads to dephosphorylation of occludin and tight junction permeability increase in LLC-PK1 epithelial cell sheets. J Cell Sci. 2000;113:3187-96.
52. Yu D, Turner JR. Stimulus-induced reorganization of tight junction structure: the role of membrane traffic. Biochim Biophys Acta. 2008;1778:709-16. (Pubitemid 351317798)
53. Ivanov AI, McCall IC, Parkos CA, Nusrat A. Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex. Mol Biol Cell. 2004;15: 2639-51. (Pubitemid 38691854)