Eicosapentaenoic Acid Enhances Heat Stress-Impaired Intestinal Epithelial Barrier Function in Caco-2 Cells

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Xiao, Guizhen ^a   Tang, Liqun ^b   Yuan, Fangfang ^b   Zhu, Wei ^a   Zhang, Shaoheng ^a   Liu, Zhifeng ^b   Geng, Yan ^b   Qiu, Xiaowen ^b   Zhang, Yali ^a   Su, Lei ^b  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b GUANGZHOU GENERAL HOSPITAL OF GUANGZHOU MILITARY COMMAND   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ARACHIDONIC ACID; ASCORBIC ACID; ENDOTOXIN; ICOSAPENTAENOIC ACID; OCCLUDIN; OMEGA 3 FATTY ACID; PROTEIN ZO1; TIGHT JUNCTION PROTEIN;

ARTICLE; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CONTROLLED STUDY; CYTOSOL; DIET SUPPLEMENTATION; ENTEROPATHY; HEAT STRESS; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; LIPID COMPOSITION; PERMEABILITY BARRIER; PROTEIN EXPRESSION; PROTEIN TRANSPORT; THERMAL EXPOSURE; TIGHT JUNCTION; WHOLE CELL;

ARACHIDONIC ACID; CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; HORSERADISH PEROXIDASE; HOT TEMPERATURE; HUMANS; INTESTINES; MICROSCOPY, ELECTRON, TRANSMISSION; TIGHT JUNCTIONS;

EID: 84884183090     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073571     Document Type: Article

References (52)

1. Turner JR, (2006) Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 169: 1901-1909.
2. Johnson LG, (2005) Applications of imaging techniques to studies of epithelial tight junctions. Adv Drug Deliv Rev 57: 111-121.
3. Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, et al. (2011) Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr 141: 769-776.
4. Bouchama A, Knochel JP, (2002) Heat stroke. N Engl J Med 346: 1978-1988.
5. Yang PC, He SH, Zheng PY, (2007) Investigation into the signal transduction pathway via which heat stress impairs intestinal epithelial barrier function. J Gastroenterol Hepatol 22: 1823-1831.
6. Lambert GP, Gisolfi CV, Berg DJ, Moseley PL, Oberley LW, et al. (2002) Selected contribution: Hyperthermia-induced intestinal permeability and the role of oxidative and nitrosative stress. J Appl Physiol 92: 1750-1761; discussion 1749.
7. Shapiro Y, Alkan M, Epstein Y, Newman F, Magazanik A, (1986) Increase in rat intestinal permeability to endotoxin during hyperthermia. Eur J Appl Physiol Occup Physiol 55: 410-412.
8. Gathiram P, Wells MT, Raidoo D, Brock-Utne JG, Gaffin SL, (1988) Portal and systemic plasma lipopolysaccharide concentrations in heat-stressed primates. Circ Shock 25: 223-230.
9. Gathiram P, Wells MT, Brock-Utne JG, Gaffin SL, (1987) Antilipopolysaccharide improves survival in primates subjected to heat stroke. Circ Shock 23: 157-164.
10. Li Q, Zhang Q, Wang M, Zhao S, Xu G, et al. (2008) n-3 polyunsaturated fatty acids prevent disruption of epithelial barrier function induced by proinflammatory cytokines. Mol Immunol 45: 1356-1365.
11. Li Q, Zhang Q, Zhang M, Wang C, Zhu Z, et al. (2008) Effect of n-3 polyunsaturated fatty acids on membrane microdomain localization of tight junction proteins in experimental colitis. FEBS J 275: 411-420.
12. Calder PC, Albers R, Antoine JM, Blum S, Bourdet-Sicard R, et al. (2009) Inflammatory disease processes and interactions with nutrition. Br J Nutr 101Suppl 1: S1-45.
13. Jiang WG, Bryce RP, Horrobin DF, Mansel RE, (1998) Regulation of tight junction permeability and occludin expression by polyunsaturated fatty acids. Biochem Biophys Res Commun 244: 414-420.
14. Caplan MS, Russell T, Xiao Y, Amer M, Kaup S, et al. (2001) Effect of polyunsaturated fatty acid (PUFA) supplementation on intestinal inflammation and necrotizing enterocolitis (NEC) in a neonatal rat model. Pediatr Res 49: 647-652.
15. Sambuy Y, De Angelis I, Ranaldi G, Scarino ML, Stammati A, et al. (2005) The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol Toxicol 21: 1-26.
16. Kang ZB, Ge Y, Chen Z, Cluette-Brown J, Laposata M, et al. (2001) Adenoviral gene transfer of Caenorhabditis elegans n-3 fatty acid desaturase optimizes fatty acid composition in mammalian cells. Proc Natl Acad Sci U S A 98: 4050-4054.
17. Roig-Perez S, Ferrer C, Rafecas M, Moreto M, Ferrer R, (2009) Correlation of taurine transport with membrane lipid composition and peroxidation in DHA-enriched Caco-2 cells. J Membr Biol 228: 141-150.
18. Bischoff SC, (2011) 'Gut health': a new objective in medicine? BMC Med 9: 24.
19. Dokladny K, Moseley PL, Ma TY, (2006) Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am J Physiol Gastrointest Liver Physiol 290: G204-212.
20. Lambert GP, Broussard LJ, Mason BL, Mauermann WJ, Gisolfi CV, (2001) Gastrointestinal permeability during exercise: effects of aspirin and energy-containing beverages. J Appl Physiol 90: 2075-2080.
21. Soeters PB, Luyer MD, Greve JW, Buurman WA, (2007) The significance of bowel permeability. Curr Opin Clin Nutr Metab Care 10: 632-638.
22. Blatteis CM, (2000) The afferent signalling of fever. J Physiol 526 Pt 3: 470.
23. Schneeberger EE, Lynch RD, (2004) The tight junction: a multifunctional complex. Am J Physiol Cell Physiol 286: C1213-1228.
24. Ferrer R, Moreno JJ, (2010) Role of eicosanoids on intestinal epithelial homeostasis. Biochem Pharmacol 80: 431-438.
25. Wong V, Gumbiner BM, (1997) A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol 136: 399-409.
26. Balda MS, Flores-Maldonado C, Cereijido M, Matter K, (2000) Multiple domains of occludin are involved in the regulation of paracellular permeability. J Cell Biochem 78: 85-96.
27. Dorfel MJ, Huber O, (2012) Modulation of tight junction structure and function by kinases and phosphatases targeting occludin. J Biomed Biotechnol 2012: 807356.
28. Kimura Y, Shiozaki H, Hirao M, Maeno Y, Doki Y, et al. (1997) Expression of occludin, tight-junction-associated protein, in human digestive tract. Am J Pathol 151: 45-54.
29. Itoh M, Nagafuchi A, Moroi S, Tsukita S, (1997) Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol 138: 181-192.
30. Dokladny K, Ye D, Kennedy JC, Moseley PL, Ma TY, (2008) Cellular and molecular mechanisms of heat stress-induced up-regulation of occludin protein expression: regulatory role of heat shock factor-1. Am J Pathol 172: 659-670.
31. Chen M, Cai H, Yang JL, Lu CL, Liu T, et al. (2008) Effect of heat stress on expression of junction-associated molecules and upstream factors androgen receptor and Wilms' tumor 1 in monkey sertoli cells. Endocrinology 149: 4871-4882.
32. Sakaguchi T, Kohler H, Gu X, McCormick BA, Reinecker HC, (2002) Shigella flexneri regulates tight junction-associated proteins in human intestinal epithelial cells. Cell Microbiol 4: 367-381.
33. Moorthy G, Murali MR, Devaraj SN, (2009) Lactobacilli facilitate maintenance of intestinal membrane integrity during Shigella dysenteriae 1 infection in rats. Nutrition 25: 350-358.
34. Strauss JG, Hayn M, Zechner R, Levak-Frank S, Frank S, (2003) Fatty acids liberated from high-density lipoprotein phospholipids by endothelial-derived lipase are incorporated into lipids in HepG2 cells. Biochem J 371: 981-988.
35. Oh IS, Shimizu H, Sato T, Uehara Y, Okada S, et al. (2005) Molecular mechanisms associated with leptin resistance: n-3 polyunsaturated fatty acids induce alterations in the tight junction of the brain. Cell Metab 1: 331-341.
36. Mullen A, Loscher CE, Roche HM, (2010) Anti-inflammatory effects of EPA and DHA are dependent upon time and dose-response elements associated with LPS stimulation in THP-1-derived macrophages. J Nutr Biochem 21: 444-450.
37. Babcock TA, Helton WS, Hong D, Espat NJ, (2002) Omega-3 fatty acid lipid emulsion reduces LPS-stimulated macrophage TNF-alpha production. Surg Infect (Larchmt) 3: 145-149.
38. Novak TE, Babcock TA, Jho DH, Helton WS, Espat NJ, (2003) NF-kappa B inhibition by omega-3 fatty acids modulates LPS-stimulated macrophage TNF-alpha transcription. Am J Physiol Lung Cell Mol Physiol 284: L84-89.
39. Mickleborough TD, Tecklenburg SL, Montgomery GS, Lindley MR, (2009) Eicosapentaenoic acid is more effective than docosahexaenoic acid in inhibiting proinflammatory mediator production and transcription from LPS-induced human asthmatic alveolar macrophage cells. Clin Nutr 28: 71-77.
40. Beutheu Youmba S, Belmonte L, Galas L, Boukhettala N, Bole-Feysot C, et al. (2012) Methotrexate modulates tight junctions through NF-kappaB, MEK, and JNK pathways. J Pediatr Gastroenterol Nutr 54: 463-470.
41. Stulnig TM, Huber J, Leitinger N, Imre EM, Angelisova P, et al. (2001) Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition. J Biol Chem 276: 37335-37340.
42. Willemsen LE, Koetsier MA, Balvers M, Beermann C, Stahl B, et al. (2008) Polyunsaturated fatty acids support epithelial barrier integrity and reduce IL-4 mediated permeability in vitro. Eur J Nutr 47: 183-191.
43. Peppelenbosch MP, Tertoolen LG, Hage WJ, de Laat SW, (1993) Epidermal growth factor-induced actin remodeling is regulated by 5-lipoxygenase and cyclooxygenase products. Cell 74: 565-575.
44. Koller M, Senkal M, Kemen M, Konig W, Zumtobel V, et al. (2003) Impact of omega-3 fatty acid enriched TPN on leukotriene synthesis by leukocytes after major surgery. Clin Nutr 22: 59-64.
45. Calder PC, (2013) Omega-3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology? Br J Clin Pharmacol 75: 645-662.
46. Bagga D, Wang L, Farias-Eisner R, Glaspy JA, Reddy ST, (2003) Differential effects of prostaglandin derived from omega-6 and omega-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion. Proc Natl Acad Sci U S A 100: 1751-1756.
47. Usami M, Muraki K, Iwamoto M, Ohata A, Matsushita E, et al. (2001) Effect of eicosapentaenoic acid (EPA) on tight junction permeability in intestinal monolayer cells. Clin Nutr 20: 351-359.
48. Usami M, Komurasaki T, Hanada A, Kinoshita K, Ohata A, (2003) 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 19: 150-156.
49. Nano JL, Nobili C, Girard-Pipau F, Rampal P, (2003) Effects of fatty acids on the growth of Caco-2 cells. Prostaglandins Leukot Essent Fatty Acids 69: 207-215.
50. Saito Y, Yokoyama M, Origasa H, Matsuzaki M, Matsuzawa Y, et al. (2008) Effects of EPA on coronary artery disease in hypercholesterolemic patients with multiple risk factors: sub-analysis of primary prevention cases from the Japan EPA Lipid Intervention Study (JELIS). Atherosclerosis 200: 135-140.
51. Singer P, Theilla M, Fisher H, Gibstein L, Grozovski E, et al. (2006) Benefit of an enteral diet enriched with eicosapentaenoic acid and gamma-linolenic acid in ventilated patients with acute lung injury. Crit Care Med 34: 1033-1038.
52. Grau-Carmona T, Moran-Garcia V, Garcia-de-Lorenzo A, Heras-de-la-Calle G, Quesada-Bellver B, et al. (2011) Effect of an enteral diet enriched with eicosapentaenoic acid, gamma-linolenic acid and anti-oxidants on the outcome of mechanically ventilated, critically ill, septic patients. Clin Nutr 30: 578-584.