594
Views
19
CrossRef citations to date
0
Altmetric
Retina

Diabetes-Induced Inflammation and Vascular Alterations in the Goto–Kakizaki Rat Retina

, , &
Pages 965-974 | Received 20 May 2019, Accepted 30 Dec 2019, Published online: 20 Jan 2020

References

  • Arden GB, Sivaprasad S. The pathogenesis of early retinal changes of diabetic retinopathy. Doc Ophthalmol. 2012;124(1):15–26. doi:10.1007/s10633-011-9305-y.
  • Wilkinson-Berka JL. Angiotensin and diabetic retinopathy. Int J Biochem Cell Biol. 2006;38(5–6):752–65. doi:10.1016/j.biocel.2005.08.002.
  • Schultze JL, Schmieder A, Goerdt S. Macrophage activation in human diseases. Semin Immunol. 2015;27(4):249–56. doi:10.1016/j.smim.2015.07.003.
  • Hachana S, Bhat M, Senecal J, Huppe-Gourgues F, Couture R, Vaucher E. Expression, distribution and function of kinin B1 receptor in the rat diabetic retina. Br J Pharmacol. 2018;175(6):968–83. doi:10.1111/bph.v175.6.
  • Altmann C, Schmidt MHH. The role of microglia in diabetic retinopathy: inflammation, microvasculature defects and neurodegeneration. Int J Mol Sci. 2018;19(1):pii: E110. doi:10.3390/ijms19010110.
  • Grigsby JG, Cardona SM, Pouw CE, Muniz A, Mendiola AS, Tsin AT, Allen DM, Cardona AE. The role of microglia in diabetic retinopathy. J Ophthalmol. 2014;2014:705783.
  • Kimura K, Toyota T, Kakizaki M, Kudo M, Takebe K, Goto Y. Impaired insulin secretion in the spontaneous diabetes rats. Tohoku J Exp Med. 1982;137(4):453–59. doi:10.1620/tjem.137.453.
  • Goto A. [Serum immunoreactive insulin after the oral administration of single dose of tolbutamide. II. Pancreatic vein immunoreactive insulin in dogs (author’s transl)]. Nihon Naibunpi Gakkai Zasshi. 1975;51(8):685–92. doi:10.1507/endocrine1927.51.8_685.
  • Portha B, Serradas P, Bailbe D, Suzuki K, Goto Y, Giroix MH. Beta-cell insensitivity to glucose in the GK rat, a spontaneous nonobese model for type II diabetes. Diabetes. 1991;40(4):486–91. doi:10.2337/diab.40.4.486.
  • Karahashi M, Hirata-Hanta Y, Kawabata K, Tsutsumi D, Kametani M, Takamatsu N, Sakamoto T, Yamazaki T, Asano S, Mitsumoto A, et al. Abnormalities in the metabolism of fatty acids and triacylglycerols in the liver of the Goto-Kakizaki rat: a model for non-obese type 2 diabetes. Lipids. 2016;51(8):955–71. doi:10.1007/s11745-016-4171-8.
  • Carmo A, Cunha-Vaz JG, Carvalho AP, Lopes MC. Nitric oxide synthase activity in retinas from non-insulin-dependent diabetic Goto-Kakizaki rats: correlation with blood-retinal barrier permeability. Nitric Oxide. 2000;4(6):590–96. doi:10.1006/niox.2000.0312.
  • Takeo-Goto S, Doi M, Ma N, Goto R, Semba R, Uji Y. Immunohistochemical localization of amino acids in the diabetic retina of Goto-Kakizaki rats. Ophthalmic Res. 2002;34:139–45.
  • Fernandes R, Suzuki K, Kumagai AK. Inner blood-retinal barrier GLUT1 in long-term diabetic rats: an immunogold electron microscopic study. Invest Ophthalmol Vis Sci. 2003;44(7):3150–54. doi:10.1167/iovs.02-1284.
  • Matsubara H, Kuze M, Sasoh M, Ma N, Furuta M, Uji Y. Time-dependent course of electroretinograms in the spontaneous diabetic Goto-Kakizaki rat. Jpn J Ophthalmol. 2006;50(3):211–16. doi:10.1007/s10384-005-0315-8.
  • Omri S, Behar-Cohen F, de Kozak Y, Sennlaub F, Verissimo LM, Jonet L, Savoldelli M, Omri B, Crisanti P. Microglia/macrophages migrate through retinal epithelium barrier by a transcellular route in diabetic retinopathy: role of PKCzeta in the Goto Kakizaki rat model. Am J Pathol. 2011;179(2):942–53. doi:10.1016/j.ajpath.2011.04.018.
  • Fan Y, Liu K, Wang Q, Ruan Y, Zhang Y, Ye W. Exendin-4 protects retinal cells from early diabetes in Goto-Kakizaki rats by increasing the Bcl-2/Bax and Bcl-xL/Bax ratios and reducing reactive gliosis. Mol Vis. 2014;20:1557–68.
  • Gong CY, Lu B, Sheng YC, Yu ZY, Zhou JY, Ji LL. The development of diabetic retinopathy in Goto-Kakizaki rat and the expression of angiogenesis-related signals. Chin J Physiol. 2016;59(2):100–08. doi:10.4077/CJP.2016.BAE383.
  • Omri S, Behar-Cohen F, Rothschild PR, Gelize E, Jonet L, Jeanny JC, Omri B, Crisanti P. PKCzeta mediates breakdown of outer blood-retinal barriers in diabetic retinopathy. PLoS One. 2013;8(11):e81600. doi:10.1371/journal.pone.0081600.
  • Miyamoto K, Ogura Y, Nishiwaki H, Matsuda N, Honda Y, Kato S, Ishida H, Seino Y. Evaluation of retinal microcirculatory alterations in the Goto-Kakizaki rat. A spontaneous model of non-insulin-dependent diabetes. Invest Ophthalmol Vis Sci. 1996;37:898–905.
  • Al-Latayfeh M, Silva PS, Sun JK, Aiello LP. Antiangiogenic therapy for ischemic retinopathies. Cold Spring Harb Perspect Med. 2012;2(6):a006411. doi:10.1101/cshperspect.a006411.
  • Pouliot M, Talbot S, Senecal J, Dotigny F, Vaucher E, Couture R. Ocular application of the kinin B1 receptor antagonist LF22-0542 inhibits retinal inflammation and oxidative stress in streptozotocin-diabetic rats. PLoS One. 2012;7(3):e33864. doi:10.1371/journal.pone.0033864.
  • Penn JS, Tolman BL, Lowery LA. Variable oxygen exposure causes preretinal neovascularization in the newborn rat. Invest Ophthalmol Vis Sci. 1993;34:576–85.
  • Kengkoom K, Klinkhamhom A, Sirimontaporn A, Singha O, Ketjareon T, Panavechkijkul Y, Seriwatanachai D, Ukong S, Ampawong S. Effects on high cholesterol-fed to liver, retina, hippocampus, and Harderian gland in Goto-Kakizaki rat. Int J Clin Exp Pathol. 2013;6:639–49.
  • Quan Y, Du J, Wang X. High glucose stimulates GRO secretion from rat microglia via ROS, PKC, and NF-kappaB pathways. J Neurosci Res. 2007;85(14):3150–59. doi:10.1002/jnr.21421.
  • Arroba AI, Alcalde-Estevez E, Garcia-Ramirez M, Cazzoni D, de la Villa P, Sanchez-Fernandez EM, Mellet CO, Garcia Fernandez JM, Hernandez C, Simo R, et al. Modulation of microglia polarization dynamics during diabetic retinopathy in db/db mice. Biochim Biophys Acta. 2016;1862(9):1663–74. doi:10.1016/j.bbadis.2016.05.024.
  • Wang W, Wang F, Lu F, Xu S, Hu W, Huang J, Gu Q, Sun X. The antiangiogenic effects of integrin alpha5beta1 inhibitor (ATN-161) in vitro and in vivo. Invest Ophthalmol Vis Sci. 2011;52(10):7213–20. doi:10.1167/iovs.10-7097.
  • Schubert HD. Cystoid macular edema: the apparent role of mechanical factors. Prog Clin Biol Res. 1989;312:277–91.
  • Ly A, Yee P, Vessey KA, Phipps JA, Jobling AI, Fletcher EL. Early inner retinal astrocyte dysfunction during diabetes and development of hypoxia, retinal stress, and neuronal functional loss. Invest Ophthalmol Vis Sci. 2011;52(13):9316–26. doi:10.1167/iovs.11-7879.
  • Abu El Asrar AM, Maimone D, Morse PH, Gregory S, Reder AT. Cytokines in the vitreous of patients with proliferative diabetic retinopathy. Am J Ophthalmol. 1992;114(6):731–36. doi:10.1016/S0002-9394(14)74052-8.
  • Yuuki T, Kanda T, Kimura Y, Kotajima N, Tamura J, Kobayashi I, Kishi S. Inflammatory cytokines in vitreous fluid and serum of patients with diabetic vitreoretinopathy. J Diabetes Complications. 2001;15(5):257–59. doi:10.1016/S1056-8727(01)00155-6.
  • Patel J. Diabetes: managing dyslipidaemia. BMJ Clin Evid. 2008;2008:pii: 0610.
  • Wilkinson-Berka JL, Fletcher EL. Angiotensin and bradykinin: targets for the treatment of vascular and neuro-glial pathology in diabetic retinopathy. Curr Pharm Des. 2004;10(27):3313–30. doi:10.2174/1381612043383179.
  • Curtis TM, Gardiner TA, Stitt AW. Microvascular lesions of diabetic retinopathy: clues towards understanding pathogenesis? Eye (Lond). 2009;23(7):1496–508. doi:10.1038/eye.2009.108.
  • Hainsworth DP, Katz ML, Sanders DA, Sanders DN, Wright EJ, Sturek M. Retinal capillary basement membrane thickening in a porcine model of diabetes mellitus. Comp Med. 2002;52:523–29.
  • Chronopoulos A, Trudeau K, Roy S, Huang H, Vinores SA, Roy S. High glucose-induced altered basement membrane composition and structure increases trans-endothelial permeability: implications for diabetic retinopathy. Curr Eye Res. 2011;36(8):747–53. doi:10.3109/02713683.2011.585735.
  • Stitt AW, Anderson HR, Gardiner TA, Archer DB. Diabetic retinopathy: quantitative variation in capillary basement membrane thickening in arterial or venous environments. Br J Ophthalmol. 1994;78(2):133–37. doi:10.1136/bjo.78.2.133.
  • Roy S, Ha J, Trudeau K, Beglova E. Vascular basement membrane thickening in diabetic retinopathy. Curr Eye Res. 2010;35(12):1045–56. doi:10.3109/02713683.2010.514659.
  • Thoumine O, Nerem RM, Girard PR. Changes in organization and composition of the extracellular matrix underlying cultured endothelial cells exposed to laminar steady shear stress. Lab Invest. 1995;73:565–76.
  • Miller CG, Budoff G, Prenner JL, Schwarzbauer JE. Minireview: fibronectin in retinal disease. Exp Biol Med (Maywood). 2017;242(1):1–7. doi:10.1177/1535370216675245.
  • Zhou T, Che D, Lan Y, Fang Z, Xie J, Gong H, Li C, Feng J, Hong H. Qi W and others. Mesenchymal marker expression is elevated in Muller cells exposed to high glucose and in animal models of diabetic retinopathy. Oncotarget. 2017;8(3):4582–94. doi:10.18632/oncotarget.13945.
  • Frank RN. Diabetic retinopathy. N Engl J Med. 2004;350(1):48–58. doi:10.1056/NEJMra021678.
  • Su EN, Alder VA, Yu DY, Yu PK, Cringle SJ, Yogesan K. Continued progression of retinopathy despite spontaneous recovery to normoglycemia in a long-term study of streptozotocin-induced diabetes in rats. Graefes Arch Clin Exp Ophthalmol. 2000;238(2):163–73. doi:10.1007/s004170050028.
  • 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(6):726–30. doi:10.1007/s001250050740.
  • Schmidt-Erfurth U, Rudolf M, Funk M, Hofmann-Rummelt C, Franz-Haas NS, Aherrahrou Z, Schlotzer-Schrehardt U. Ultrastructural changes in a murine model of graded bruch membrane lipoidal degeneration and corresponding VEGF164 detection. Invest Ophthalmol Vis Sci. 2008;49(1):390–98. doi:10.1167/IOVS.07-0227.
  • Joyal JS, Sun Y, Gantner ML, Shao Z, Evans LP, Saba N, Fredrick T, Burnim S, Kim JS. Patel G and others. Retinal lipid and glucose metabolism dictates angiogenesis through the lipid sensor Ffar1. Nat Med. 2016;22(4):439–45. doi:10.1038/nm.4059.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.