Remodeling of retinal fatty acids in an animal model of diabetes: A decrease in long-chain polyunsaturated fatty acids is associated with a decrease in fatty acid elongases Elovl2 and Elovl4

Diabetes

Volumn 59, Issue 1, 2010, Pages 219-227

  Tikhonenko, Maria ^a   Lydic, Todd A ^a   Wang, Yun ^b   Chen, Weiqin ^c   Opreanu, Madalina ^a,d   Sochacki, Andrew ^a   McSorley, Kelly M ^a   Renis, Rebecca L ^a   Kern, Timothy ^e   Jump, Donald B ^f   Reid, Gavin E ^a,g   Busik, Julia V ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b GTx   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d Case Western Reserve University ^*  (United States)

^e CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f OREGON STATE UNIVERSITY   (United States)

^g Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOCOSAHEXAENOIC ACID; ELONGASE; GLUCOSE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; LIVER ENZYME; PHOSPHATIDYLCHOLINE; POLYUNSATURATED FATTY ACID; STREPTOZOCIN; UNCLASSIFIED DRUG; VASCULOTROPIN; ACYLTRANSFERASE; FATTY ACID ELONGASES; LIPID; PHOSPHOLIPID; UNSATURATED FATTY ACID; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FATTY ACID METABOLISM; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA; STREPTOZOCIN DIABETES; WEIGHT GAIN; ANIMAL; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

ACETYLTRANSFERASES; ANIMALS; BLOOD GLUCOSE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIABETES MELLITUS, EXPERIMENTAL; FATTY ACIDS, UNSATURATED; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INTERCELLULAR ADHESION MOLECULE-1; LIPIDS; MALE; PHOSPHOLIPIDS; RATS; RATS, SPRAGUE-DAWLEY; RETINA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WEIGHT GAIN;

EID: 77449154762     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0728     Document Type: Article

References (49)

1. Schroder S, Palinski W, Schmid-Schonbein GW. Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy. Am J Pathol 1991;139:81-100
2. Miyamoto K, Khosrof S, Bursell SE, Rohan R, Murata T, Clermont AC, Aiello LP, Ogura Y, Adamis AP. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci U S A 1999;96:10836-10841
3. Adamis AP. Is diabetic retinopathy an inflammatory disease? Br J Ophthalmol 2002;86:363-365
4. Yang LP, Sun HL, Wu LM, Guo XJ, Dou HL, Tso MO, Zhao L, Li SM. Baicalein reduces inflammatory process in a rodent model of diabetic retinopathy. Invest Ophthalmol Vis Sci 2009;50:2319-2327
5. Sone H, Kawakami Y, Okuda Y, Sekine Y, Honmura S, Matsuo K, Segawa T, Suzuki H, Yamashita K. Ocular vascular endothelial growth factor levels in diabetic rats are elevated before observable retinal proliferative changes. Diabetologia 1997;40:726-730
6. Nozaki M, Ogura Y, Hirabayashi Y, Saishin Y, Shimada S. Enhanced expression of adhesion molecules of the retinal vascular endothelium in spontaneous diabetic rats. Ophthalmic Res 2002;34:158-164
7. Al-Shabrawey M, Rojas M, Sanders T, Behzadian A, El-Remessy A, Bartoli M, Parpia AK, Liou G, Caldwell RB. Role of NADPH oxidase in retinal vascular inflammation. Invest Ophthalmol Vis Sci 2008;49:3239-3244
8. Joussen AM, Poulaki V, Mitsiades N, Kirchhof B, Koizumi K, Dohmen S, Adamis AP. Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF-alpha suppression. FASEB J 2002;16:438-440
9. Gustavsson C, Agardh CD, Hagert P, Agardh E. Inflammatory markers in nondiabetic and diabetic rat retinas exposed to ischemia followed by reperfusion. Retina 2008;28:645-652
10. Lyons TJ, Jenkins AJ, Zheng D, Lackland DT, McGee D, Garvey WT, Klein RL. Diabetic retinopathy and serum lipoprotein subclasses in the DCCT/EDIC cohort. Invest Ophthalmol Vis Sci 2004;45:910-918
11. Coppack SW, Evans RD, Fisher RM, Frayn KN, Gibbons GF, Humphreys SM, Kirk ML, Potts JL, Hockaday TD. Adipose tissue metabolism in obesity: lipase action in vivo before and after a mixed meal. Metabolism 1992;41:264-272
12. Weinstock PH, Levak-Frank S, Hudgins LC, Radner H, Friedman JM, Zechner R, Breslow JL. Lipoprotein lipase controls fatty acid entry into adipose tissue, but fat mass is preserved by endogenous synthesis in mice deficient in adipose tissue lipoprotein lipase. Proc Natl Acad Sci U S A 1997;94:10261-10266
13. Julius U. Influence of plasma free fatty acids on lipoprotein synthesis and diabetic dyslipidemia. Exp Clin Endocrinol Diabetes 2003;111:246-250
14. Sprecher H, Chen Q. Polyunsaturated fatty acid biosynthesis: a microsomal-peroxisomal process. Prostaglandins Leukot Essent Fatty Acids 1999; 60:317-321 (Pubitemid 29401786)
15. Agbaga MP, Brush RS, Mandal MN, Henry K, Elliott MH, Anderson RE. Role of Stargardt-3 macular dystrophy protein (ELOVL4) in the biosynthesis of very long chain fatty acids. Proc Natl Acad Sci U S A 2008;105:12843-12848
16. Lagali PS, Liu J, Ambasudhan R, Kakuk LE, Bernstein SL, Seigel GM, Wong PW, Ayyagari R. Evolutionarily conserved ELOVL4 gene expression in the vertebrate retina. Invest Ophthalmol Vis Sci 2003;44:2841-2850
17. Umeda S, Ayyagari R, Suzuki MT, Ono F, Iwata F, Fujiki K, Kanai A, Takada Y, Yoshikawa Y, Tanaka Y, Iwata T. Molecular cloning of ELOVL4 gene from cynomolgus monkey (Macaca fascicularis). Exp Anim 2003;52:129-135
18. Zhang XM, Yang Z, Karan G, Hashimoto T, Baehr W, Yang XJ, Zhang K. Elovl4 mRNA distribution in the developing mouse retina and phylogenetic conservation of Elovl4 genes. Mol Vis 2003;9:301-307
19. Grayson C, Molday RS. Dominant negative mechanism underlies autosomal dominant Stargardt-like macular dystrophy linked to mutations in ELOVL4. J Biol Chem 2005;280:32521-32530
20. Karan G, Lillo C, Yang Z, Cameron DJ, Locke KG, Zhao Y, Thirumalaichary S, Li C, Birch DG, Vollmer-Snarr HR, Williams DS, Zhang K. Lipofuscin accumulation, abnormal electrophysiology, and photoreceptor degeneration in mutant ELOVL4 transgenic mice: a model for macular degeneration. Proc Natl Acad Sci U S A 2005;102:4164-4169
21. Zhang K, Kniazeva M, Han M, Li W, Yu Z, Yang Z, Li Y, Metzker ML, Allikmets R, Zack DJ, Kakuk LE, Lagali PS, Wong PW, MacDonald IM, Sieving PA, Figueroa DJ, Austin CP, Gould RJ, Ayyagari R, Petrukhin K. A 5-bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy. Nat Genet 2001;27:89-93
22. Brenner RR. Hormonal modulation of delta6 and delta5 desaturases: case of diabetes. Prostaglandins Leukot Essent Fatty Acids 2003;68:151-162
23. Nakamura MT, Nara TY. Gene regulation of mammalian desaturases. Biochem Soc Trans 2002;30:1076-1079
24. Rimoldi OJ, Finarelli GS, Brenner RR. Effects of diabetes and insulin on hepatic delta6 desaturase gene expression. Biochem Biophys Res Commun 2001;283:323-326
25. Wang Y, Botolin D, Xu J, Christian B, Mitchell E, Jayaprakasam B, Nair MG, Peters JM, Busik JV, Olson LK, Jump DB. Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity. J Lipid Res 2006;47:2028-2041
26. Meyer A, Kirsch H, Domergue F, Abbadi A, Sperling P, Bauer J, Cirpus P, Zank TK, Moreau H, Roscoe TJ, Zahringer U, Heinz E. Novel fatty acid elongases and their use for the reconstitution of docosahexaenoic acid biosynthesis. J Lipid Res 2004;45:1899-1909
27. Anderson RE. Lipids of ocular tissues: IV. A comparison of the phospholipids from the retina of six mammalian species. Exp Eye Res 1970;10:339-344
28. Chen W, Esselman WJ, Jump DB, Busik JV. Anti-inflammatory effect of docosahexaenoic acid on cytokine-induced adhesion molecule expression in human retinal vascular endothelial cells. Invest Ophthalmol Vis Sci 2005;46:4342-4347
29. Lydic TA, Busik JV, Esselman WJ, Reid GE. Complementary precursor ion and neutral loss scan mode tandem mass spectrometry for the analysis of glycerophosphatidylethanolamine lipids from whole rat retina. Anal Bioanal Chem 2009;394:267-275
30. Murphy EJ, Stephens R, Jurkowitz-Alexander M, Horrocks LA. Acidic hydrolysis of plasmalogens followed by high-performance liquid chromatography. Lipids 1993;28:565-568
31. Rose H, Oklander M. An improved method for the extraction of lipids from human erythrocytes. J Lipid Res 1965;6:428-443
32. Han X, Gross RW. Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom Rev 2005;24:367-412
33. Haimi P, Uphoff A, Hermansson M, Somerharju P. Software tools for analysis of mass spectrometric lipidome data. Anal Chem 2006;78:8324-8331
34. Futterman S, Sturtevant R, Kupfer C. Effect of alloxan diabetes on the fatty acid composition of the retina. Invest Ophthalmol 1969;8:542-544
35. Hegde KR, Varma SD. Electron impact mass spectroscopic studies on mouse retinal fatty acids: effect of diabetes. Ophthalmic Res 2009;42:9-14
36. Harbige LS. Fatty acids, the immune response, and autoimmunity: a question of n-6 essentiality and the balance between n-6 and n-3. Lipids 2003;38:323-341
37. Chen W, Jump DB, Grant MB, Esselman WJ, Busik JV. Dyslipidemia, but not hyperglycemia, induces inflammatory adhesion molecules in human retinal vascular endothelial cells. Invest Ophthalmol Vis Sci 2003;44:5016-5022
38. Joussen AM, Poulaki V, Qin W, Kirchhof B, Mitsiades N, Wiegand SJ, Rudge J, Yancopoulos GD, Adamis AP. Retinal vascular endothelial growth factor induces intercellular adhesion molecule-1 and endothelial nitric oxide synthase expression and initiates early diabetic retinal leukocyte adhesion in vivo. Am J Pathol 2002;160:501-509
39. Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol 2001;158:147-152
40. Lu M, Perez VL, Ma N, Miyamoto K, Peng HB, Liao JK, Adamis AP. VEGF increases retinal vascular ICAM-1 expression in vivo. Invest Ophthalmol Vis Sci 1999;40:1808-1812
41. Funatsu H, Yamashita H, Shimizu E, Kojima R, Hori S. Relationship between vascular endothelial growth factor and interleukin-6 in diabetic retinopathy. Retina 2001;21:469-477
42. Fliesler SJ, Anderson RE. Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 1983;22:79-131
43. Delton-Vandenbroucke I, Grammas P, Anderson RE. Polyunsaturated fatty acid metabolism in retinal and cerebral microvascular endothelial cells. J Lipid Res 1997;38:147-159
44. Moon YA, Shah NA, Mohapatra S, Warrington JA, Horton JD. Identification of a mammalian long chain fatty acyl elongase regulated by sterol regulatory element-binding proteins. J Biol Chem 2001;276:45358-45366
45. Jakobsson A, Westerberg R, Jacobsson A. Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res 2006;45:237-249
46. Leonard AE, Pereira SL, Sprecher H, Huang YS. Elongation of long-chain fatty acids. Prog Lipid Res 2004;43:36-54
47. Sunada S, Kiyose C, Kubo K, Takebayashi J, Sanada H, Saito M. Effect of docosahexaenoic acid intake on lipid peroxidation in diabetic rat retina under oxidative stress. Free Radic Res 2006;40:837-846
48. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes: early onset and effect of insulin. J Clin Invest 1998;102:783-791
49. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Nakamura M. New insights into the pathophysiology of diabetic retinopathy: potential cell-specific therapeutic targets. Diabetes Technol Ther 2000;2:601-608