Skip to main content
Top
Published in: Graefe's Archive for Clinical and Experimental Ophthalmology 2/2012

01-02-2012 | Basic Science

Polyunsaturated fatty acids induce modification in the lipid composition and the prostaglandin production of the conjunctival epithelium cells

Authors: Sabrina Viau, Laurent Leclère, Bénédicte Buteau, Stéphane Grégoire, Niyazi Acar, Alain Bron, Catherine P. Creuzot-Garcher, Lionel Bretillon, Corinne Joffre

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 2/2012

Login to get access

Abstract

Background

This study was conducted to evaluate whether polyunsaturated fatty acids (PUFA) such as γ-linolenic acid (GLA) and eicosapentaenoic acid (EPA), as found in the diet, may affect the lipid composition of conjunctival epithelium and whether these modifications affect prostaglandin (PG) production after inflammatory stimulation.

Methods

Chang and IOBA-NHC conjunctival human cells were treated with GLA and/or EPA at 5, 10, 20, 30, 40, or 50 μg/ml for 72 h and then were stimulated with interferon-gamma (IFN-γ) for 48 h. Changes in the composition of neutral lipids and phospholipids were monitored by gas chromatography. PGE1 and PGE2 levels were measured by enzyme immunoassay.

Results

PUFA supplementations in the culture medium induced incorporation of these fatty acids and of their metabolites in neutral lipids and phospholipids of the conjunctival cells. The fatty acid composition of neutral lipids and phospholipids was not affected by stimulation with IFN-γ. The production of PGE1 and PGE2 was affected by GLA supplementation whereas it was not modified by EPA supplementation. A combined supplementation of EPA and GLA did not change the production of PGE1 but decreased the production of PGE2.

Conclusions

These results suggest that modulation of fatty acid composition and PG production by PUFA supplementation is possible in the conjunctival epithelium, which is an important site of inflammation in dry eye syndrome.
Literature
1.
go back to reference Bourre JM (2006) Effects of nutrients (in food) on the structure and function of the nervous system: update on dietary requirements for brain. Part 2: macronutrients. J Nutr Health Aging 10:386–99PubMed Bourre JM (2006) Effects of nutrients (in food) on the structure and function of the nervous system: update on dietary requirements for brain. Part 2: macronutrients. J Nutr Health Aging 10:386–99PubMed
2.
go back to reference Schnebelen C, Pasquis B, Salinas-Navarro M, Joffre C, Creuzot-Garcher CP, Vidal-Sanz M, Bron AM, Bretillon L, Acar N (2009) A dietary combination of omega-3 and omega-6 polyunsaturated fatty acids is more efficient than single supplementations in the prevention of retinal damage induced by elevation of intraocular pressure in rats. Graefes Arch Clin Exp Ophthalmol Schnebelen C, Pasquis B, Salinas-Navarro M, Joffre C, Creuzot-Garcher CP, Vidal-Sanz M, Bron AM, Bretillon L, Acar N (2009) A dietary combination of omega-3 and omega-6 polyunsaturated fatty acids is more efficient than single supplementations in the prevention of retinal damage induced by elevation of intraocular pressure in rats. Graefes Arch Clin Exp Ophthalmol
3.
go back to reference Schnebelen C, Viau S, Gregoire S, Joffre C, Creuzot-Garcher CP, Bron AM, Bretillon L, Acar N (2009) Nutrition for the eye: different susceptibility of the retina and the lacrimal gland to dietary omega-6 and omega-3 polyunsaturated fatty acid incorporation. Ophthalmic Res 41:216–24PubMedCrossRef Schnebelen C, Viau S, Gregoire S, Joffre C, Creuzot-Garcher CP, Bron AM, Bretillon L, Acar N (2009) Nutrition for the eye: different susceptibility of the retina and the lacrimal gland to dietary omega-6 and omega-3 polyunsaturated fatty acid incorporation. Ophthalmic Res 41:216–24PubMedCrossRef
4.
go back to reference Viau S, Maire MA, Pasquis B, Gregoire S, Acar N, Bron AM, Bretillon L, Creuzot-Garcher CP, Joffre C (2009) Efficacy of a 2-month dietary supplementation with polyunsaturated fatty acids in dry eye induced by scopolamine in a rat model. Graefes Arch Clin Exp Ophthalmol 247:1039–50PubMedCrossRef Viau S, Maire MA, Pasquis B, Gregoire S, Acar N, Bron AM, Bretillon L, Creuzot-Garcher CP, Joffre C (2009) Efficacy of a 2-month dietary supplementation with polyunsaturated fatty acids in dry eye induced by scopolamine in a rat model. Graefes Arch Clin Exp Ophthalmol 247:1039–50PubMedCrossRef
5.
go back to reference Barham JB, Edens MB, Fonteh AN, Johnson MM, Easter L, Chilton FH (2000) Addition of eicosapentaenoic acid to gamma-linolenic acid-supplemented diets prevents serum arachidonic acid accumulation in humans. J Nutr 130:1925–31PubMed Barham JB, Edens MB, Fonteh AN, Johnson MM, Easter L, Chilton FH (2000) Addition of eicosapentaenoic acid to gamma-linolenic acid-supplemented diets prevents serum arachidonic acid accumulation in humans. J Nutr 130:1925–31PubMed
6.
go back to reference Miles EA, Banerjee T, Calder PC (2004) The influence of different combinations of gamma-linolenic, stearidonic and eicosapentaenoic acids on the fatty acid composition of blood lipids and mononuclear cells in human volunteers. Prostaglandins, Leukot Essent Fatty Acids 70:529–38CrossRef Miles EA, Banerjee T, Calder PC (2004) The influence of different combinations of gamma-linolenic, stearidonic and eicosapentaenoic acids on the fatty acid composition of blood lipids and mononuclear cells in human volunteers. Prostaglandins, Leukot Essent Fatty Acids 70:529–38CrossRef
7.
go back to reference Calder PC (2006) n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83:1505S–1519SPubMed Calder PC (2006) n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83:1505S–1519SPubMed
8.
go back to reference Culp BR, Titus BG, Lands WE (1979) Inhibition of prostaglandin biosynthesis by eicosapentaenoic acid. Prostaglandins Med 3:269–78PubMedCrossRef Culp BR, Titus BG, Lands WE (1979) Inhibition of prostaglandin biosynthesis by eicosapentaenoic acid. Prostaglandins Med 3:269–78PubMedCrossRef
9.
go back to reference Schnebelen C, Gregoire S, Pasquis B, Joffre C, Creuzot-Garcher CP, Bron AM, Bretillon L, Acar N (2009) Dietary n-3 and n-6 PUFA enhance DHA incorporation in retinal phospholipids without affecting PGE(1) and PGE (2) levels. Lipids 44:465–70PubMedCrossRef Schnebelen C, Gregoire S, Pasquis B, Joffre C, Creuzot-Garcher CP, Bron AM, Bretillon L, Acar N (2009) Dietary n-3 and n-6 PUFA enhance DHA incorporation in retinal phospholipids without affecting PGE(1) and PGE (2) levels. Lipids 44:465–70PubMedCrossRef
10.
go back to reference Stern ME, Pflugfelder SC (2004) Inflammation in dry eye. Ocul Surf 2:124–30PubMed Stern ME, Pflugfelder SC (2004) Inflammation in dry eye. Ocul Surf 2:124–30PubMed
11.
go back to reference Aragona P, Bucolo C, Spinella R, Giuffrida S, Ferreri G (2005) Systemic omega-6 essential fatty acid treatment and pge1 tear content in Sjögren's syndrome patients. Invest Ophthalmol Vis Sci 46:4474–9PubMedCrossRef Aragona P, Bucolo C, Spinella R, Giuffrida S, Ferreri G (2005) Systemic omega-6 essential fatty acid treatment and pge1 tear content in Sjögren's syndrome patients. Invest Ophthalmol Vis Sci 46:4474–9PubMedCrossRef
12.
go back to reference Barabino S, Rolando M, Camicione P, Ravera G, Zanardi S, Giuffrida S, Calabria G (2003) Systemic linoleic and gamma-linolenic acid therapy in dry eye syndrome with an inflammatory component. Cornea 22:97–101PubMedCrossRef Barabino S, Rolando M, Camicione P, Ravera G, Zanardi S, Giuffrida S, Calabria G (2003) Systemic linoleic and gamma-linolenic acid therapy in dry eye syndrome with an inflammatory component. Cornea 22:97–101PubMedCrossRef
13.
14.
go back to reference Macri A, Giuffrida S, Amico V, Iester M, Traverso CE (2003) Effect of linoleic acid and gamma-linolenic acid on tear production, tear clearance and on the ocular surface after photorefractive keratectomy. Graefes Arch Clin Exp Ophthalmol 241:561–6PubMedCrossRef Macri A, Giuffrida S, Amico V, Iester M, Traverso CE (2003) Effect of linoleic acid and gamma-linolenic acid on tear production, tear clearance and on the ocular surface after photorefractive keratectomy. Graefes Arch Clin Exp Ophthalmol 241:561–6PubMedCrossRef
15.
go back to reference Wojtowicz JC, Butovich I, Uchiyama E, Aronowicz J, Agee S, McCulley JP (2011) Pilot, prospective, randomized, double-masked, placebo-controlled clinical trial of an omega-3 supplement for dry eye. Cornea 30:308–14PubMedCrossRef Wojtowicz JC, Butovich I, Uchiyama E, Aronowicz J, Agee S, McCulley JP (2011) Pilot, prospective, randomized, double-masked, placebo-controlled clinical trial of an omega-3 supplement for dry eye. Cornea 30:308–14PubMedCrossRef
16.
go back to reference Miljanovic B, Trivedi KA, Dana MR, Gilbard JP, Buring JE, Schaumberg DA (2005) Relation between dietary n-3 and n-6 fatty acids and clinically diagnosed dry eye syndrome in women. Am J Clin Nutr 82:887–93PubMed Miljanovic B, Trivedi KA, Dana MR, Gilbard JP, Buring JE, Schaumberg DA (2005) Relation between dietary n-3 and n-6 fatty acids and clinically diagnosed dry eye syndrome in women. Am J Clin Nutr 82:887–93PubMed
17.
go back to reference Leventhal LJ, Boyce EG, Zurier RB (1993) Treatment of rheumatoid arthritis with gammalinolenic acid. Ann Intern Med 119:867–73PubMed Leventhal LJ, Boyce EG, Zurier RB (1993) Treatment of rheumatoid arthritis with gammalinolenic acid. Ann Intern Med 119:867–73PubMed
18.
go back to reference Kulkarni PS, Srinivasan BD (1989) Cyclooxygenase and lipoxygenase pathways in anterior uvea and conjunctiva. Prog Clin Biol Res 312:39–52PubMed Kulkarni PS, Srinivasan BD (1989) Cyclooxygenase and lipoxygenase pathways in anterior uvea and conjunctiva. Prog Clin Biol Res 312:39–52PubMed
19.
go back to reference Goustard-Langelier B, Alessandri JM, Raguenez G, Durand G, Courtois Y (2000) Phospholipid incorporation and metabolic conversion of n-3 polyunsaturated fatty acids in the Y79 retinoblastoma cell line. J Neurosci Res 60:678–85PubMedCrossRef Goustard-Langelier B, Alessandri JM, Raguenez G, Durand G, Courtois Y (2000) Phospholipid incorporation and metabolic conversion of n-3 polyunsaturated fatty acids in the Y79 retinoblastoma cell line. J Neurosci Res 60:678–85PubMedCrossRef
20.
go back to reference Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509PubMed Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509PubMed
21.
go back to reference Juaneda P, Rocquelin G (1985) Rapid and convenient separation of phospholipids and non-phosphorus lipids from rat heart using silica cartridges. Lipids 20:40–41PubMedCrossRef Juaneda P, Rocquelin G (1985) Rapid and convenient separation of phospholipids and non-phosphorus lipids from rat heart using silica cartridges. Lipids 20:40–41PubMedCrossRef
22.
go back to reference Joffre C, Souchier M, Gregoire S, Viau S, Bretillon L, Acar N, Bron AM, Creuzot-Garcher C (2008) Differences in meibomian fatty acid composition in patients with meibomian gland dysfunction and aqueous-deficient dry eye. Br J Ophthalmol 92:116–9PubMedCrossRef Joffre C, Souchier M, Gregoire S, Viau S, Bretillon L, Acar N, Bron AM, Creuzot-Garcher C (2008) Differences in meibomian fatty acid composition in patients with meibomian gland dysfunction and aqueous-deficient dry eye. Br J Ophthalmol 92:116–9PubMedCrossRef
23.
go back to reference Wang Y, Botolin D, Xu J, Christian B, Mitchell E, Jayaprakasam B, Nair MG, Peters JM, Busik JV, Olson LK, Jump DB (2006) Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity. J Lipid Res 47:2028–41PubMedCrossRef Wang Y, Botolin D, Xu J, Christian B, Mitchell E, Jayaprakasam B, Nair MG, Peters JM, Busik JV, Olson LK, Jump DB (2006) Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity. J Lipid Res 47:2028–41PubMedCrossRef
24.
go back to reference Zheng X, Torstensen BE, Tocher DR, Dick JR, Henderson RJ, Bell JG (2005) Environmental and dietary influences on highly unsaturated fatty acid biosynthesis and expression of fatty acyl desaturase and elongase genes in liver of Atlantic salmon (Salmo salar). Biochim Biophys Acta 1734:13–24PubMed Zheng X, Torstensen BE, Tocher DR, Dick JR, Henderson RJ, Bell JG (2005) Environmental and dietary influences on highly unsaturated fatty acid biosynthesis and expression of fatty acyl desaturase and elongase genes in liver of Atlantic salmon (Salmo salar). Biochim Biophys Acta 1734:13–24PubMed
25.
go back to reference Nakamura MT, Nara TY (2004) Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr 24:345–76PubMedCrossRef Nakamura MT, Nara TY (2004) Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr 24:345–76PubMedCrossRef
26.
go back to reference Williard DE, Kaduce TL, Harmon SD, Spector AA (1998) Conversion of eicosapentaenoic acid to chain-shortened omega-3 fatty acid metabolites by peroxisomal oxidation. J Lipid Res 39:978–86PubMed Williard DE, Kaduce TL, Harmon SD, Spector AA (1998) Conversion of eicosapentaenoic acid to chain-shortened omega-3 fatty acid metabolites by peroxisomal oxidation. J Lipid Res 39:978–86PubMed
27.
go back to reference Sprecher H, Luthria DL, Mohammed BS, Baykousheva SP (1995) Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. J Lipid Res 36:2471–7PubMed Sprecher H, Luthria DL, Mohammed BS, Baykousheva SP (1995) Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. J Lipid Res 36:2471–7PubMed
28.
go back to reference Obata T, Nagakura T, Masaki T, Maekawa K, Yamashita K (1999) Eicosapentaenoic acid inhibits prostaglandin D2 generation by inhibiting cyclo-oxygenase-2 in cultured human mast cells. Clin Exp Allergy 29:1129–35PubMedCrossRef Obata T, Nagakura T, Masaki T, Maekawa K, Yamashita K (1999) Eicosapentaenoic acid inhibits prostaglandin D2 generation by inhibiting cyclo-oxygenase-2 in cultured human mast cells. Clin Exp Allergy 29:1129–35PubMedCrossRef
29.
go back to reference Herman CA, Hamberg M, Granstrom E (1987) Quantitative determination of prostaglandins E1, E2 and E3 in frog tissue. J Chromatogr 394:353–62PubMedCrossRef Herman CA, Hamberg M, Granstrom E (1987) Quantitative determination of prostaglandins E1, E2 and E3 in frog tissue. J Chromatogr 394:353–62PubMedCrossRef
30.
go back to reference Raisz LG, Alander CB, Simmons HA (1989) Effects of prostaglandin E3 and eicosapentaenoic acid on rat bone in organ culture. Prostaglandins 37:615–25PubMedCrossRef Raisz LG, Alander CB, Simmons HA (1989) Effects of prostaglandin E3 and eicosapentaenoic acid on rat bone in organ culture. Prostaglandins 37:615–25PubMedCrossRef
31.
go back to reference Rubin D, Laposata M (1991) Regulation of agonist-induced prostaglandin E1 versus prostaglandin E2 production. A mass analysis J Biol Chem 266:23618–23 Rubin D, Laposata M (1991) Regulation of agonist-induced prostaglandin E1 versus prostaglandin E2 production. A mass analysis J Biol Chem 266:23618–23
32.
go back to reference He J, Bazan HE (2010) Omega-3 fatty acids in dry eye and corneal nerve regeneration after refractive surgery. Prostaglandins Leukot Essent Fatty Acids 82:319–25PubMedCrossRef He J, Bazan HE (2010) Omega-3 fatty acids in dry eye and corneal nerve regeneration after refractive surgery. Prostaglandins Leukot Essent Fatty Acids 82:319–25PubMedCrossRef
33.
go back to reference Mukherjee PK, Chawla A, Loayza MS, Bazan NG (2007) Docosanoids are multifunctional regulators of neural cell integrity and fate: significance in aging and disease. Prostaglandins Leukot Essent Fatty Acids 77:233–8PubMedCrossRef Mukherjee PK, Chawla A, Loayza MS, Bazan NG (2007) Docosanoids are multifunctional regulators of neural cell integrity and fate: significance in aging and disease. Prostaglandins Leukot Essent Fatty Acids 77:233–8PubMedCrossRef
34.
go back to reference Serhan CN, Chiang N (2008) Endogenous pro-resolving and anti-inflammatory lipid mediators: a new pharmacologic genus. Br J Pharmacol 153(Suppl 1):S200–15PubMed Serhan CN, Chiang N (2008) Endogenous pro-resolving and anti-inflammatory lipid mediators: a new pharmacologic genus. Br J Pharmacol 153(Suppl 1):S200–15PubMed
35.
go back to reference Li N, He J, Schwartz CE, Gjorstrup P, Bazan HE (2010) Resolvin E1 improves tear production and decreases inflammation in a dry eye mouse model. J Ocul Pharmacol Ther 26:431–9PubMedCrossRef Li N, He J, Schwartz CE, Gjorstrup P, Bazan HE (2010) Resolvin E1 improves tear production and decreases inflammation in a dry eye mouse model. J Ocul Pharmacol Ther 26:431–9PubMedCrossRef
36.
go back to reference Christman JW, Lancaster LH, Blackwell TS (1998) Nuclear factor kappa B: a pivotal role in the systemic inflammatory response syndrome and new target for therapy. Intensive Care Med 24:1131–8PubMedCrossRef Christman JW, Lancaster LH, Blackwell TS (1998) Nuclear factor kappa B: a pivotal role in the systemic inflammatory response syndrome and new target for therapy. Intensive Care Med 24:1131–8PubMedCrossRef
37.
go back to reference Zhao Y, Joshi-Barve S, Barve S, Chen LH (2004) Eicosapentaenoic acid prevents LPS-induced TNF-alpha expression by preventing NF-kappaB activation. J Am Coll Nutr 23:71–8PubMed Zhao Y, Joshi-Barve S, Barve S, Chen LH (2004) Eicosapentaenoic acid prevents LPS-induced TNF-alpha expression by preventing NF-kappaB activation. J Am Coll Nutr 23:71–8PubMed
38.
go back to reference Tsubota K, Fukagawa K, Fujihara T, Shimmura S, Saito I, Saito K, Takeuchi T (1999) Regulation of human leukocyte antigen expression in human conjunctival epithelium. Invest Ophthalmol Vis Sci 40:28–34PubMed Tsubota K, Fukagawa K, Fujihara T, Shimmura S, Saito I, Saito K, Takeuchi T (1999) Regulation of human leukocyte antigen expression in human conjunctival epithelium. Invest Ophthalmol Vis Sci 40:28–34PubMed
39.
go back to reference Lavappa KS, Macy ML, Shannon JE (1976) Examination of ATCC stocks for HeLa marker chromosomes in human cell lines. Nature 259:211–3PubMedCrossRef Lavappa KS, Macy ML, Shannon JE (1976) Examination of ATCC stocks for HeLa marker chromosomes in human cell lines. Nature 259:211–3PubMedCrossRef
40.
go back to reference Guenoun JM, Baudouin C, Rat P, Pauly A, Warnet JM, Brignole-Baudouin F (2005) In vitro comparison of cytoprotective and antioxidative effects of latanoprost, travoprost, and bimatoprost on conjunctiva-derived epithelial cells. Invest Ophthalmol Vis Sci 46:4594–9PubMedCrossRef Guenoun JM, Baudouin C, Rat P, Pauly A, Warnet JM, Brignole-Baudouin F (2005) In vitro comparison of cytoprotective and antioxidative effects of latanoprost, travoprost, and bimatoprost on conjunctiva-derived epithelial cells. Invest Ophthalmol Vis Sci 46:4594–9PubMedCrossRef
41.
go back to reference Diebold Y, Calonge M, Enriquez de Salamanca A, Callejo S, Corrales RM, Saez V, Siemasko KF, Stern ME (2003) Characterization of a spontaneously immortalized cell line (IOBA-NHC) from normal human conjunctiva. Invest Ophthalmol Vis Sci 44:4263–74PubMedCrossRef Diebold Y, Calonge M, Enriquez de Salamanca A, Callejo S, Corrales RM, Saez V, Siemasko KF, Stern ME (2003) Characterization of a spontaneously immortalized cell line (IOBA-NHC) from normal human conjunctiva. Invest Ophthalmol Vis Sci 44:4263–74PubMedCrossRef
Metadata
Title
Polyunsaturated fatty acids induce modification in the lipid composition and the prostaglandin production of the conjunctival epithelium cells
Authors
Sabrina Viau
Laurent Leclère
Bénédicte Buteau
Stéphane Grégoire
Niyazi Acar
Alain Bron
Catherine P. Creuzot-Garcher
Lionel Bretillon
Corinne Joffre
Publication date
01-02-2012
Publisher
Springer-Verlag
Published in
Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 2/2012
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI
https://doi.org/10.1007/s00417-011-1801-y

Other articles of this Issue 2/2012

Graefe's Archive for Clinical and Experimental Ophthalmology 2/2012 Go to the issue