Chronic insulin treatment of diabetes does not fully normalize alterations in the retinal transcriptome

BMC Medical Genomics

Volumn 4, Issue , 2011, Pages

  Bixler, Georgina V ^a   Vanguilder, Heather D ^a   Brucklacher, Robert M ^a   Kimball, Scot R ^a   Bronson, Sarah K ^a   Freeman, Willard M ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; EYE PROTEIN; GLUCOSE; INSULIN; JANUS KINASE 3; MESSENGER RNA; PROTEIN LITAF; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DIABETIC RETINOPATHY; GENE EXPRESSION PROFILING; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENETIC VARIABILITY; GENOME ANALYSIS; GLUCOSE BLOOD LEVEL; INSULIN TREATMENT; MALE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STREPTOZOCIN DIABETES; TRANSCRIPTOMICS; ANIMAL; BIOMETRY; DIABETES MELLITUS; DNA MICROARRAY; DNA PROBE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; REPRODUCIBILITY; RETINA; SPRAGUE DAWLEY RAT;

RATTUS; RODENTIA;

ANIMALS; BIOMETRY; DIABETES MELLITUS; DNA PROBES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; INSULIN; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS; RETINA; RNA, MESSENGER;

EID: 79955821526     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/1755-8794-4-40     Document Type: Article

References (54)

1. Preserving human vision: eliminating blindness from diabetes mellitus. LM Aiello, J Am Optom Assoc 1998 69 690 692 9844319
2. Risk factors for high-risk proliferative diabetic retinopathy and severe visual loss: Early Treatment Diabetic Retinopathy Study Report #18. MD Davis MR Fisher RE Gangnon F Barton LM Aiello EY Chew FL Ferris GL Knatterud, Invest Ophthalmol Vis Sci 1998 39 233 252 9477980 (Pubitemid 28093859)
3. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. Diabetes Control and Complications Trial Research Group, N Engl J Med 1993 329 977 986 8366922
4. Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy. The Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. DCCT/EDIC STudy Group, N Engl J Med 2000 342 381 389 10666428
5. Prolonged effect of intensive therapy on the risk of retinopathy complications in patients with type 1 diabetes mellitus: 10 years after the Diabetes Control and Complications Trial. NH White W Sun PA Cleary RP Danis MD Davis DP Hainsworth LD Hubbard JM Lachin DM Nathan, Arch Ophthalmol 2008 126 1707 1715 19064853
6. 10-year follow-up of intensive glucose control in type 2 diabetes. RR Holman SK Paul MA Bethel DR Matthews HA Neil, N Engl J Med 2008 359 1577 1589 10.1056/NEJMoa0806470 18784090
7. Progression of incipient diabetic retinopathy during good glycemic control. RL Engerman TS Kern, Diabetes 1987 36 808 812 10.2337/diabetes.36.7.808 3556280 (Pubitemid 17145301)
8. Islet transplantation inhibits diabetic retinopathy in the sucrose-fed diabetic Cohen rat. HP Hammes I Klinzing S Wiegand RG Bretzel AM Cohen K Federlin, Invest Ophthalmol Vis Sci 1993 34 2092 2096 8491559 (Pubitemid 23148648)
9. Resistance of retinal inflammatory mediators to suppress after reinstitution of good glycemic control: novel mechanism for metabolic memory. PS Chan M Kanwar RA Kowluru, J Diabetes Complications 2010 24 55 63 10.1016/j.jdiacomp.2008.10.002 19056300
10. Re-institution of good metabolic control in diabetic rats and activation of caspase-3 and nuclear transcriptional factor (NF-kappaB) in the retina. RA Kowluru S Chakrabarti S Chen, Acta Diabetol 2004 41 194 199 10.1007/s00592-004- 0165-8 15660203 (Pubitemid 40174996)
11. Metabolic memory phenomenon and accumulation of peroxynitrite in retinal capillaries. RA Kowluru M Kanwar A Kennedy, Exp Diabetes Res 2007 2007 21976 17641740
12. Overexpression of fibronectin induced by diabetes or high glucose: phenomenon with a memory. S Roy R Sala E Cagliero M Lorenzi, Proc Natl Acad Sci USA 1990 87 404 408 10.1073/pnas.87.1.404 2296596
13. Metabolic memory in diabetes is true long-term memory. RN Frank, Arch Ophthalmol 2009 127 330 331 10.1001/archophthalmol.2008.607 19273799
14. Whole genome assessment of the retinal response to diabetes reveals a progressive neurovascular inflammatory response. RM Brucklacher KM Patel HD VanGuilder GV Bixler AJ Barber DA Antonetti CM Lin KF LaNoue TW Gardner SK Bronson,, et al. BMC Med Genomics 2008 1 26 10.1186/1755-8794-1-26 18554398
15. The retinal proteome in experimental diabetic retinopathy: up-regulation of crystallins and reversal by systemic and periocular insulin. PE Fort WM Freeman MK Losiewicz RS Singh TW Gardner, Mol Cell Proteomics 2009 8 767 779 10.1074/mcp.M800326-MCP200 19049959
16. A multistep validation process of biomarkers for preclinical drug development. WM Freeman GV Bixler RM Brucklacher CM Lin KM Patel HD VanGuilder KF LaNoue SR Kimball AJ Barber DA Antonetti,, et al. Pharmacogenomics J 2010 10 385 395 10.1038/tpj.2009.60 19997081
17. Transcriptomic comparison of the retina in two mouse models of diabetes. WM Freeman GV Bixler RM Brucklacher E Walsh SR Kimball LS Jefferson SK Bronson, J Ocul Biol Dis Infor 2009 2 202 213 10.1007/s12177-009-9045-3 20157355
18. Multi-modal proteomic analysis of retinal protein expression alterations in a rat model of diabetic retinopathy. HD VanGuilder GV Bixler L Kutzler RM Brucklacher SK Bronson SR Kimball WM Freeman, Plos One 2011 6 16271 10.1371/journal.pone.0016271
19. Microarray data analysis: from disarray to consolidation and consensus. DB Allison X Cui GP Page M Sabripour, Nat Rev Genet 2006 7 55 65 10.1038/nrg1749 16369572 (Pubitemid 41828948)
20. On testing the signicance of sets of genes. B Efron R Tibshirani, Annals of Applied Statistics 2006 1 107 129
21. Aging alters the expression of neurotransmission-regulating proteins in the hippocampal synaptoproteome. HD VanGuilder H Yan JA Farley WE Sonntag WM Freeman, J Neurochem 2010 113 1577 1588 20374424
22. Expression of acute-phase response proteins in retinal Muller cells in diabetes. C Gerhardinger MB Costa MC Coulombe I Toth T Hoehn P Grosu, Invest Ophthalmol Vis Sci 2005 46 349 357 10.1167/iovs.04-0860 15623795 (Pubitemid 40041218)
23. Immune regulation in the retina. B Detrick JJ Hooks, Immunol Res 2010 47 153 161 10.1007/s12026-009-8146-1 20082152
24. Cloning and chromosomal mapping of mouse ladinin, a novel basement membrane zone component. K Motoki M Megahed S LaForgia J Uitto, Genomics 1997 39 323 330 10.1006/geno.1996.4507 9119369 (Pubitemid 27078698)
25. MED14 and MED1 differentially regulate target-specific gene activation by the glucocorticoid receptor. W Chen I Rogatsky MJ Garabedian, Mol Endocrinol 2006 20 560 572 16239257 (Pubitemid 43291208)
26. Differential gene expression patterns by oligonucleotide microarray of basal versus lipopolysaccharide-activated monocytes from cord blood versus adult peripheral blood. H Jiang D Van P Satwani LV Baxi MS Cairo, J Immunol 2004 172 5870 5879 15128766 (Pubitemid 38655936)
27. Metallothionein protects retinal pigment epithelial cells against apoptosis and oxidative stress. H Lu DM Hunt R Ganti A Davis K Dutt J Alam RC Hunt, Exp Eye Res 2002 74 83 92 10.1006/exer.2001.1101 11878821 (Pubitemid 34948268)
28. Modulation of retinal capillary endothelial cells by Muller glial cell-derived factors. H Abukawa M Tomi J Kiyokawa S Hori T Kondo T Terasaki K Hosoya, Mol Vis 2009 15 451 457 19247458
29. A novel lipopolysaccharide-induced transcription factor regulating tumor necrosis factor alpha gene expression: molecular cloning, sequencing, characterization, and chromosomal assignment. F Myokai S Takashiba R Lebo S Amar, Proc Natl Acad Sci USA 1999 96 4518 4523 10.1073/pnas.96.8.4518 10200294 (Pubitemid 29190368)
30. Molecular cloning and characterization of mouse LITAF cDNA: role in the regulation of tumor necrosis factor-alpha (TNF-alpha) gene expression. AL Bolcato-Bellemin MG Mattei M Fenton S Amar, J Endotoxin Res 2004 10 15 23 15025820 (Pubitemid 38461248)
31. Thioredoxin interacting protein (TXNIP) induces inflammation through chromatin modification in retinal capillary endothelial cells under diabetic conditions. L Perrone TS Devi K Hosoya T Terasaki LP Singh, J Cell Physiol 2009 221 262 272 10.1002/jcp.21852 19562690
32. Inhibition of TXNIP expression in vivo blocks early pathologies of diabetic retinopathy. L Perrone TS Devi K-I Hosoya T Terasaki LP Singh, Cell Death and Disease 2010 1
33. Interaction of 11-cis-retinol dehydrogenase with the chromophore of retinal g protein-coupled receptor opsin. P Chen TD Lee HK Fong, J Biol Chem 2001 276 21098 21104 10.1074/jbc.M010441200 11274198
34. An opsin homologue in the retina and pigment epithelium. M Jiang S Pandey HK Fong, Invest Ophthalmol Vis Sci 1993 34 3669 3678 8258527 (Pubitemid 24012007)
35. Evaluation of the role of the retinal G protein-coupled receptor (RGR) in the vertebrate retina in vivo. T Maeda JP Van Hooser CA Driessen S Filipek JJ Janssen K Palczewski, J Neurochem 2003 85 944 956 10.1046/j.1471-4159.2003. 01741.x 12716426 (Pubitemid 36578626)
36. Role of histone acetylation in the development of diabetic retinopathy and the metabolic memory phenomenon. Q Zhong RA Kowluru, J Cell Biochem 2010 110 1306 1313 10.1002/jcb.22644 20564224
37. Epigenetic phenomena linked to diabetic complications. L Pirola A Balcerczyk J Okabe A El-Osta, Nat Rev Endocrinol 2010
38. Leukocyte attraction through the CCR5 receptor controls progress from insulitis to diabetes in non-obese diabetic mice. C Carvalho-Pinto MI Garcia L Gomez A Ballesteros A Zaballos JM Flores M Mellado JM Rodriguez-Frade D Balomenos A Martinez, Eur J Immunol 2004 34 548 557 10.1002/eji.200324285 14768060 (Pubitemid 39272795)
39. Suppressive effect of insulin infusion on chemokines and chemokine receptors. H Ghanim K Korzeniewski CL Sia S Abuaysheh T Lohano A Chaudhuri P Dandona, Diabetes Care 2010 33 1103 1108 10.2337/dc09-2193 20200310
40. Relation of circulating concentrations of chemokine receptor CCR5 ligands to C-peptide, proinsulin and HbA1c and disease progression in type 1 diabetes. C Pfleger A Kaas L Hansen B Alizadeh P Hougaard R Holl H Kolb BO Roep HB Mortensen NC Schloot, Clin Immunol 2008 128 57 65 10.1016/j.clim.2008.03.458 18434252
41. The differential role of Jak/STAT signaling in retinal degeneration. C Lange M Thiersch M Samardzija C Grimm, Adv Exp Med Biol 2010 664 601 607 10.1007/978-1-4419-1399-9-69 20238064
42. Quinolinic acid phosphoribosyltransferase in human and rat brain: activity in Huntington's disease and in quinolinate-lesioned rat striatum. AC Foster WO Whetsell Jr ED Bird R Schwarcz, Brain Res 1985 336 207 214 10.1016/0006-8993(85)90647-X 3159462 (Pubitemid 15008370)
43. Differential activities, subcellular distribution and tissue expression patterns of three members of Slingshot family phosphatases that dephosphorylate cofilin. Y Ohta K Kousaka K Nagata-Ohashi K Ohashi A Muramoto Y Shima R Niwa T Uemura K Mizuno, Genes Cells 2003 8 811 824 10.1046/j.1365-2443.2003.00678.x 14531860 (Pubitemid 37304357)
44. Increased alpha 2-macroglobulin in diabetes: a hyperglycemia related phenomenon associated with reduced antithrombin III activity. A Ceriello D Giugliano A Quatraro A Stante RP Dello R Torella, Acta Diabetol Lat 1989 26 147 154 10.1007/BF02581366 2476904 (Pubitemid 19210735)
45. Immunohistochemical localization of low density lipoprotein receptor-related protein 1 and alpha(2)-Macroglobulin in retinal and choroidal tissue of proliferative retinopathies. PF Barcelona JD Luna GA Chiabrando CP Juarez IA Bhutto T Baba DS McLeod MC Sanchez GA Lutty, Exp Eye Res 2010 91 264 272 10.1016/j.exer.2010.05.017 20561980
46. Vascular damage in a mouse model of diabetic retinopathy: relation to neuronal and glial changes. RA Feit-Leichman R Kinouchi M Takeda Z Fan S Mohr TS Kern DF Chen, Invest Ophthalmol Vis Sci 2005 46 4281 4287 10.1167/iovs.04-1361 16249509 (Pubitemid 44264633)
47. Retinal glial cell immunoreactivity and neuronal cell changes in rats with STZ-induced diabetes. E Agardh A Bruun CD Agardh, Curr Eye Res 2001 23 276 284 10.1076/ceyr.23.4.276.5459 11852429 (Pubitemid 34161300)
48. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes. The Penn State Retina Research Group. AJ Barber DA Antonetti TW Gardner, Invest Ophthalmol Vis Sci 2000 41 3561 3568 11006253
49. Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. LR Potter S bbey-Hosch DM Dickey, Endocr Rev 2006 27 47 72 16291870 (Pubitemid 43228238)
50. The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. N Matsukawa WJ Grzesik N Takahashi KN Pandey S Pang M Yamauchi O Smithies, Proc Natl Acad Sci USA 1999 96 7403 7408 10.1073/pnas.96.13.7403 10377427 (Pubitemid 29299674)
51. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. TS Kern, Exp Diabetes Res 2007 2007 95103 18274606
52. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. DA Antonetti AJ Barber SK Bronson WM Freeman TW Gardner LS Jefferson M Kester SR Kimball JK Krady KF LaNoue,, et al. Diabetes 2006 55 2401 2411 10.2337/db05-1635 16936187 (Pubitemid 44871140)
53. Strain-dependent increases in retinal inflammatory proteins and photoreceptor FGF-2 expression in streptozotocin-induced diabetic rats. SJ Kirwin ST Kanaly NA Linke JL Edelman, Invest Ophthalmol Vis Sci 2009 50 5396 5404 10.1167/iovs.09-3474 19474406
54. The role of epigenetics in the pathology of diabetic complications. LM Villeneuve R Natarajan, Am J Physiol Renal Physiol 2010 299 14 F25 10.1152/ajprenal.00200.2010 20462972