Early adaptive response of the retina to a pro-diabetogenic diet: Impairment of cone response and gene expression changes in high-fructose fed rats

Experimental Eye Research

Volumn 135, Issue , 2015, Pages 37-46

  Thierry, Magalie ^a,b   Pasquis, Bruno ^a,b   Buteau, Bénédicte ^a,b   Fourgeux, Cynthia ^a,b   Dembele, Doulaye ^c,d   Leclere, Laurent ^a,b   Gambert Nicot, Ségolène ^a,b,e   Acar, Niyazi ^a,b   Bron, Alain M ^a,b,e   Creuzot Garcher, Catherine P ^a,b,e   Bretillon, Lionel ^a,b  

^a CEMAGREF   (France)

^b CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e DIJON UNIVERSITY HOSPITAL   (France)

Author keywords

Diet; Electroretinography; Fructose; Gene expression; Retina

Indexed keywords

ALPHA CRYSTALLIN; CHOLESTEROL; CRYSTALLIN; FRUCTOSAMINE; FRUCTOSE; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LEPTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN; PROTEIN ELF2; PROTEIN ELF4; S6 KINASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CARBOHYDRATE DIET; GLUCOSE BLOOD LEVEL; INITIATION FACTOR 2;

ANIMAL EXPERIMENT; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETOGENESIS; DIET; ELECTRORETINOGRAPHY; END2 GENE; ENDOPLASMIC RETICULUM STRESS; FRUCTOSAMINE BLOOD LEVEL; GENE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; INSULIN BLOOD LEVEL; INSULINEMIA; LIGHT INTENSITY; MALE; MITOCHONDRION; NID1 GENE; NONHUMAN; NPY GENE; OPTC GENE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; RETINA; RETINA CONE; RETINA ROD; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; ADMINISTRATION AND DOSAGE; ANALYSIS; ANIMAL; BLOOD; CARBOHYDRATE DIET; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BLOOD GLUCOSE; CHOLESTEROL; CRYSTALLINS; DIABETES MELLITUS, EXPERIMENTAL; DIET; DIETARY CARBOHYDRATES; ELECTRORETINOGRAPHY; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC INITIATION FACTOR-2; FRUCTOSAMINE; FRUCTOSE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INSULIN; LEPTIN; MALE; RATS; RETINA; RETINAL CONE PHOTORECEPTOR CELLS;

EID: 84928614294     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.04.012     Document Type: Article

References (51)

1. Abari E., Kociok N., Hartmann U., Semkova I., Paulsson M., Lo A., Joussen A.M. Alterations in basement membrane immunoreactivity of the diabetic retina in three diabetic mouse models. Graefes Arch. Clin. Exp. Ophthalmol. 2013, 251:763-775.
2. Abcouwer S.F., Gardner T.W. Diabetic retinopathy: loss of neuroretinal adaptation to the diabetic metabolic environment. Ann. N. Y. Acad. Sci. 2014, 1311:174-190.
3. Alberti K.G.M.M., Eckel R.H., Grundy S.M., Zimmet P.Z., Cleeman J.I., Donato K.A., Fruchart J.-C., James W.P.T., Loria C.M., Smith S.C. Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, Lung, and blood Institute; American heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation 2009, 120:1640-1645.
4. Andley U.P. Crystallins in the eye: function and pathology. Prog. Retin Eye Res. 2007, 26:78-98.
5. Antonetti D.A., Barber A.J., Bronson S.K., Freeman W.M., Gardner T.W., Jefferson L.S., Kester M., Kimball S.R., Krady J.K., LaNoue K.F., Norbury C.C., Quinn P.G., Sandirasegarane L., Simpson I.A. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes 2006, 55:2401-2411.
6. Arrigo A.P., Simon S., Gibert B., Kretz-Remy C., Nivon M., Czekalla A., Guillet D., Moulin M., Diaz-Latoud C., Vicart P. Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett. 2007, 581:3665-3674.
7. Aydin S., Aksoy A., Aydin S., Kalayci M., Yilmaz M., Kuloglu T., Citil C., Catak Z. Today's and yesterday's of pathophysiology: biochemistry of metabolic syndrome and animal models. Nutrition 2014, 30:1-9.
8. Balasubramani M., Schreiber E.M., Candiello J., Balasubramani G.K., Kurtz J., Halfter W. Molecular interactions in the retinal basement membrane system: a proteomic approach. Matrix Biol. 2010, 29:471-483.
9. Benani A., Hryhorczuk C., Gouazé A., Fioramonti X., Brenachot X., Guissard C., Krezymon A., Duparc T., Colom A., Nédélec E., Rigault C., Lemoine A., Gascuel J., Gerardy-Schahn R., Valet P., Knauf C., Lorsignol A., Pénicaud L. Food intake adaptation to dietary fat involves PSA-dependent rewiring of the arcuate melanocortin system in mice. J.Neurosci. 2012, 32:11970-11979.
10. Bhat S.P., Nagineni C.N. alpha B subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem. Biophys. Res. Commun. 1989, 158:319-325.
11. Biel M., Seeliger M., Pfeifer A., Kohler K., Gerstner A., Ludwig A., Jaissle G., Fauser S., Zrenner E., Hofmann F. Selective loss of cone function in mice lacking the cyclic nucleotide-gated channel CNG3. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7553-7557.
12. Bursać B.N., Vasiljević A.D., Nestorović N.M., Veličković N.A., Vojnović Milutinović D.D., Matić G.M., Djordjevic A.D. High-fructose diet leads to visceral adiposity and hypothalamic leptin resistance in male rats - do glucocorticoids play a role?. J.Nutr. Biochem. 2014, 25:446-455.
13. Calvo-Ochoa E., Hernandez-Ortega K., Ferrera P., Morimoto S., Arias C. Short-term high-fat-and-fructose feeding produces insulin signaling alterations accompanied by neurite and synaptic reduction and astroglial activation in the rat hippocampus. J.Cereb. Blood Flow. Metab. 2014, 34:1001-1008.
14. Cho K.I., Haque M., Wang J., Yu M., Hao Y., Qiu S., Pillai I.C., Peachey N.S., Ferreira P.A. Distinct and atypical intrinsic and extrinsic cell death pathways between photoreceptor cell types upon specific ablation of Ranbp2 in cone photoreceptors. PLoS Genet. 2013, 9:e1003555.
15. Darwin C. On the Origin of Species by Means of Natural Selection 1859.
16. Dekker M.J., Su Q., Baker C., Rutledge A.C., Adeli K. Fructose: a highly lipogenic nutrient implicated in insulin resistance, hepatic steatosis, and the metabolic syndrome. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E685-E694.
17. Delbosc S., Paizanis E., Magous R., Araiz C., Dimo T., Cristol J.P., Cros G., Azay J. Involvement of oxidative stress and NADPH oxidase activation in the development of cardiovascular complications in a model of insulin resistance, the fructose-fed rat. Atherosclerosis 2005, 179:43-49.
18. Dembele D., Kastner P. Fold change rank ordering statistics: a new method for detecting differentially expressed genes. BMC Bioinforma. 2014, 15:14.
19. Di Polo A., Cheng L., Bray G.M., Aguayo A.J. Colocalization of TrkB and brain-derived neurotrophic factor proteins in Green-Red-Sensitive cone outer segments. Invest Ophthalmol. Vis. Sci. 2000, 41:4014-4021.
20. Fort P.E., Freeman W.M., Losiewicz M.K., Singh R.S., Gardner T.W. The retinal proteome in experimental diabetic retinopathy: up-regulation of crystallins and reversal by systemic and periocular insulin. Mol. Cell. Proteomics 2009, 8:767-779.
21. Fourgeux C., Martine L., Pasquis B., Maire M.A., Acar N., Creuzot-Garcher C., Bron A., Bretillon L. Steady-state levels of 24S-hydroxycholesterol are maintained by glial cells intervention after elevation of intraocular pressure in the rat. Acta Ophthalmol. 2012, 90:e560-e564.
22. Hancock H.A., Kraft T.W. Oscillatory potential analysis and ERGs of Normal and diabetic rats. Invest Ophthalmol. Vis. Sci. 2004, 45:1002-1008.
23. Heise E.A., Marozas L.M., Grafton S.A., Green K.M., Kirwin S.J., Fort P.E. Strain-independent increases of crystallin proteins in the retina of type 1 diabetic rats. PLoS One 2013, 8:e82520.
24. Jaissle G.B., May C.A., Reinhard J., Kohler K., Fauser S., Lutjen-Drecoll E., Zrenner E., Seeliger M.W. Evaluation of the rhodopsin knockout mouse as a model of pure cone function. Invest. Ophthalmol. Vis. Sci. 2001, 42:506-513.
25. Kannan R., Sreekumar P.G., Hinton D.R. Novel roles for alpha-crystallins in retinal function and disease. Prog. Retin Eye Res. 2012, 31:576-604.
26. Kase S., Ishida S., Rao N.A. Increased expression of alphaA-crystallin in human diabetic eye. Int. J. Mol. Med. 2011, 28:505-511.
27. Keenan T.D.L., Clark S.J., Unwin R.D., Ridge L.A., Day A.J., Bishop P.N. Mapping the differential distribution of proteoglycan Core proteins in the adult human retina, choroid, and sclera. Invest Ophthalmol. Vis. Sci. 2012, 53:7528-7538.
28. Kim Y.H., Choi M.Y., Kim Y.S., Han J.M., Lee J.H., Park C.H., Kang S.S., Choi W.S., Cho G.J. Protein kinase C δ regulates anti-apoptotic αB-crystallin in the retina of type 2 diabetes. Neurobiol. Dis. 2007, 28:293-303.
29. Le Goff M.M., Lu H., Ugarte M., Henry S., Takanosu M., Mayne R., Bishop P.N. The vitreous glycoprotein opticin inhibits preretinal neovascularization. Invest Ophthalmol. Vis. Sci. 2012, 53:228-234.
30. Losiewicz M.K., Fort P.E. Diabetes impairs the neuroprotective properties of retinal alpha-crystallins. Invest Ophthalmol. Vis. Sci. 2011, 52:5034-5042.
31. Marmor M.F., Fulton A.B., Holder G.E., Miyake Y., Brigell M., Bach M., International Society for Clinical Electrophysiology of, V ISCEV standard for full-field clinical electroretinography (2008 update). Doc. Ophthalmol. 2009, 118:69-77.
32. Masilamoni J.G., Jesudason E.P., Bharathi S.N., Jayakumar R. The protective effect of alpha-crystallin against acute inflammation in mice. Biochim. Biophys. Acta 2005, 1740:411-420.
33. Qian H., Shah M.R., Alexander K.R., Ripps H. Two distinct processes are evident in rat cone flicker ERG responses at low and high temporal frequencies. Exp. Eye Res. 2008, 87:71-75.
34. Rattner A., Nathans J. The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia. J.Neurosci. 2005, 25:4540-4549.
35. Samardzija M., Wariwoda H., Imsand C., Huber P., Heynen S.R., Gubler A., Grimm C. Activation of survival pathways in the degenerating retina of rd10 mice. Exp. Eye Res. 2012, 99:17-26.
36. Schmitt U., Tanimoto N., Seeliger M., Schaeffel F., Leube R.E. Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 2009, 162:234-243.
37. Seeliger M.W., Grimm C., Stahlberg F., Friedburg C., Jaissle G., Zrenner E., Guo H., Reme C.E., Humphries P., Hofmann F., Biel M., Fariss R.N., Redmond T.M., Wenzel A. New views on RPE65 deficiency: the rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat. Genet. 2001, 29:70-74.
38. Semkova I., Kociok N., Karagiannis D., Nischt R., Smyth N., Paulsson M., Strauß O., Joussen A.M. Anti-angiogenic effect of the basement membrane protein nidogen-1 in a mouse model of choroidal neovascularization. Exp. Eye Res. 2014, 118:80-88.
39. Sinha D., Klise A., Sergeev Y., Hose S., Bhutto I.A., Hackler L., Malpic-Llanos T., Samtani S., Grebe R., Goldberg M.F., Hejtmancik J.F., Nath A., Zack D.J., Fariss R.N., McLeod D.S., Sundin O., Broman K.W., Lutty G.A., Zigler J.S. betaA3/A1-crystallin in astroglial cells regulates retinal vascular remodeling during development. Mol. Cell. Neurosci. 2008, 37:85-95.
40. Stranahan A.M., Norman E.D., Lee K., Cutler R.G., Telljohann R.S., Egan J.M., Mattson M.P. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 2008, 18:1085-1088.
41. Templeton J.P., Wang X., Freeman N.E., Ma Z., Lu A., Hejtmancik F., Geisert E.E. Acrystallin gene network in the mouse retina. Exp. Eye Res. 2013, 116:129-140.
42. Thanos S., Naskar R. Correlation between retinal ganglion cell death and chronically developing inherited glaucoma in a new rat mutant. Exp. Eye Res. 2004, 79:119-129.
43. Thierry M., Pasquis B., Acar N., Grégoire S., Febvret V., Buteau B., Gambert-Nicot S., Bron A., Creuzot-Garcher C., Bretillon L. Metabolic syndrome triggered by high-fructose diet favors choroidal neovascularization and impairs retinal light sensitivity in the rat. PLoS One 2014, 9:e112450.
44. Van Hooser J.P., Liang Y., Maeda T., Kuksa V., Jang G.-F., He Y.-G., Rieke F., Fong H.K.W., Detwiler P.B., Palczewski K. Recovery of visual functions in a mouse model of Leber congenital amaurosis. J.Biol. Chem. 2002, 277:19173-19182.
45. VanGuilder H.D., Bixler G.V., Kutzler L., Brucklacher R.M., Bronson S.K., Kimball S.R., Freeman W.M. Multi-modal proteomic analysis of retinal protein expression alterations in a rat model of diabetic retinopathy. PLoS One 2011, 6:e16271.
46. Venkatesh A., Ma S., Le Y.Z., Hall M.N., Rüegg M.A., Punzo C. Activated mTORC1 promotes long-term cone survival in retinitis pigmentosa mice. J.Clin. Invest 2015, 125:1446-1458.
47. Verginelli F., Aru F., Battista P., Mariani-Costantini R. Nutrigenetics in the light of human evolution. J.Nutr. Nutr. 2009, 2:91-102.
48. Xu J., Morris L.M., Michalakis S., Biel M., Fliesler S.J., Sherry D.M., Ding X.Q. CNGA3 deficiency affects cone synaptic terminal structure and function and leads to secondary rod dysfunction and degeneration. Invest Ophthalmol. Vis. Sci. 2012, 53:1117-1129.
49. Yang R.B., Robinson S.W., Xiong W.H., Yau K.W., Birch D.G., Garbers D.L. Disruption of a retinal guanylyl cyclase gene leads to cone-specific dystrophy and paradoxical rod behavior. J.Neurosci. 1999, 19:5889-5897.
50. Zhang C., Gehlbach P., Gongora C., Cano M., Fariss R., Hose S., Nath A., Green W.R., Goldberg M.F., Zigler J.S., Sinha D. Apotential role for beta- and gamma-crystallins in the vascular remodeling of the eye. Dev. Dyn. 2005, 234:36-47.
51. Zhang K., Yao G., Gao Y., Hofeldt K.J., Lei B. Frequency spectrum and amplitude analysis of dark- and light-adapted oscillatory potentials in albino mouse, rat and rabbit. Doc. Ophthalmol. 2007, 115:85-93.