Animal Models of Diabetic Retinopathy

Current Diabetes Reports - Tập 17 - Trang 1-17 - 2017
Ana Maria Olivares1, Kristen Althoff1, Gloria Fanghua Chen1, Siqi Wu1, Margaux A. Morrisson2, Margaret M. DeAngelis2, Neena Haider1
1Schepens Eye Research Institute, Massachusetts Eye and Ear Infirmary, Department of Ophthalmology, Harvard Medical School, Boston, USA
2Moran Eye Center, University of Utah, Salt Lake City, USA

Tóm tắt

Diabetic retinopathy (DR) is one of the most common complications associated with chronic hyperglycemia seen in patients with diabetes mellitus. While many facets of DR are still not fully understood, animal studies have contributed significantly to understanding the etiology and progression of human DR. This review provides a comprehensive discussion of the induced and genetic DR models in different species and the advantages and disadvantages of each model. Rodents are the most commonly used models, though dogs develop the most similar morphological retinal lesions as those seen in humans, and pigs and zebrafish have similar vasculature and retinal structures to humans. Nonhuman primates can also develop diabetes mellitus spontaneously or have focal lesions induced to simulate retinal neovascular disease observed in individuals with DR. DR results in vascular changes and dysfunction of the neural, glial, and pancreatic β cells. Currently, no model completely recapitulates the full pathophysiology of neuronal and vascular changes that occur at each stage of diabetic retinopathy; however, each model recapitulates many of the disease phenotypes.

Tài liệu tham khảo

Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet [Internet]. 2010;376(9735):124–36. Available from: http://www.sciencedirect.com/science/article/pii/S0140673609621243 .

Lee R, Wong TY, Sabanayagam C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis [Internet] London BioMed Central. 2015;2:17. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4657234/.

Yau JWY, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care [Internet]. Am Diabetes Assoc. 2012;35(3):556–64. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3322721/.

Rabb MF, Gagliano DA, Sweeney HE. Diabetic retinopathy in Blacks. Diabetes Care [Internet]. 1990;13(11):1202 LP–1206. Available from: http://care.diabetesjournals.org/content/13/11/1202.abstract.

Aiello LP, Gardner TW, King GL, Blankenship G, Cavallerano JD, Ferris FL, et al. Diabetic retinopathy. Diabetes Care [Internet]. 1998;21(1):143 LP–156. Available from: http://care.diabetesjournals.org/content/21/1/143.abstract.

Haffner SM, Fong D, Stern MP, Pugh JA, Hazuda HP, Patterson JK, et al. Diabetic retinopathy in Mexican Americans and non-Hispanic Whites. Diabetes [Internet]. 1988;37(7):878 LP–884. Available from: http://diabetes.diabetesjournals.org/content/37/7/878.abstract.

Haffner SM, Mitchell BD, Moss SE, Stern MP, Hazuda HP, Patterson J, et al. Is there an ethnic difference in the effect of risk factors for diabetic retinopathy? Ann Epidemiol [Internet]. 1993;3(1):2–8. Available from: http://www.sciencedirect.com/science/article/pii/104727979390003M.

Wong T, Klein R, Islam F, Cotch M, Folsom A, Klein B, et al. Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol [Internet]. 2006;141(3):446–55. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2246042/.

Liew G, Klein R, Wong TY. The role of genetics in susceptibility to diabetic retinopathy. Int Ophthalmol Clin [Internet]. 2009;49(2):35–52. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2746819/.

Haffner SM, Hazuda HP, Stern MP, Patterson JK, WAJ VH, Fong D. Effect of socioeconomic status on hyperglycemia and retinopathy levels in Mexican Americans with NIDDM. Diabetes Care [Internet]. 1989;12(2):128 LP–134. Available from: http://care.diabetesjournals.org/content/12/2/128.abstract.

•• Cho H, Sobrin L. Genetics of diabetic retinopathy. Curr Diab Rep [Internet]. 2014;14(8):515. doi:10.1007/s11892-014-0515-z. This is an important reference because it provides insight on how genetics plays a role in diabetic retinopathy. Understanding this will give more information on future development of therapies for treatment of this area.

Karalliedde J, Gnudi L. Diabetes mellitus, a complex and heterogeneous disease, and the role of insulin resistance as a determinant of diabetic kidney disease. Nephrol Dial Transplant [Internet]. 2016;31(2):206–13. doi:10.1093/ndt/gfu405.

Kowluru RA, Santos JM, Mishra M. Epigenetic modifications and diabetic retinopathy. Biomed Res Int Hindawi Publishing Corporation; 2013;2013.

Torres JM, Cox NJ, Philipson LH. Genome wide association studies for diabetes: perspective on results and challenges. Pediatr Diabetes Wiley Online Library. 2013;14(2):90–6.

Madsen-Bouterse SA, Kowluru RA. Oxidative stress and diabetic retinopathy: pathophysiological mechanisms and treatment perspectives. Rev Endocr Metab Disord Springer. 2008;9(4):315–27.

Santos JM, Tewari S, Goldberg AFX, Kowluru RA. Mitochondrial biogenesis and the development of diabetic retinopathy. Free Radic Biol Med Elsevier. 2011;51(10):1849–60.

Madsen-Bouterse SA, Mohammad G, Kanwar M, Kowluru RA. Role of mitochondrial DNA damage in the development of diabetic retinopathy, and the metabolic memory phenomenon associated with its progression. Antioxid Redox Signal [Internet]. 140 Huguenot Street, 3rd FloorNew Rochelle, NY 10801USA: Mary Ann Liebert, Inc.; 2010 15;13(6):797–805 Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2935337/.

Nentwich MM, Ulbig MW. Diabetic retinopathy—ocular complications of diabetes mellitus. World J Diabetes [Internet] Baishideng Publishing Group Inc. 2015;6(3):489–99. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4398904/.

Cunha-Vaz J. Characterization and relevance of different diabetic retinopathy phenotypes. Dev Ophthalmol. 2007;39:13–30.

Robinson R, Barathi VA, Chaurasia SS, Wong TY, Kern TS. Update on animal models of diabetic retinopathy: from molecular approaches to mice and higher mammals. Dis Model Mech [Internet] Company Biologists Limited. 2012;5(4):444–56. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3380708/.

Makino S, Kunimoto K, Muraoka Y, Mizushima Y, Katagiri K, Tochino Y. Breeding of a non-obese, diabetic strain of mice. Jikken Dobutsu. 1980;29:1–13.

Thayer TC, Wilson BS, Mathews CE. Use of NOD mice to understand human type 1 diabetes. Endocrinol Metab Clin North Am [Internet]. 2010;39(3):541–61. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2925291/.

• Pearson JA, Wong FS, Wen L. The importance of the non obese diabetic (NOD) mouse model in autoimmune diabetes. J Autoimmun [Internet]. 2016;66:76–88. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4765310/. The article discusses the use of a nonobese diabetic animal model. The use of this model has helped uncover the significance of environmental factors in the DR disease. It is also an important model to understanding autoimmune diseases in diabetes and identify the role of the immune system in disease progression.

Hummel KP, Dickie MM, Coleman DL. Diabetes, a new mutation in the mouse. Science (80- ) [Internet]. 1966;153(3740):1127 LP–1128. Available from: http://science.sciencemag.org/content/153/3740/1127.abstract.

Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, et al. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell [Internet]. 1996;84(3):491–5. Available from: http://www.sciencedirect.com/science/article/pii/S0092867400812945.

Miyamoto K, Hiroshiba N, Tsujikawa A, Ogura Y. In vivo demonstration of increased leukocyte entrapment in retinal microcirculation of diabetic rats. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 1998;39(11):2190–4.

Lai AKW, Lo ACY. Animal models of diabetic retinopathy: summary and comparison. J Diabetes Res. Hindawi Publishing Corporation; 2013;2013.

Engerman RL, Bloodworth JMB. Experimental diabetic retinopathy in dogs. Arch Ophthalmol Am Med Assoc. 1965;73(2):205–10.

Kador PF, Takahashi Y, Wyman M, Ferris F. Diabeteslike proliferative retinal changes in galactose-fed dogs. Arch Ophthalmol Am Med Assoc. 1995;113(3):352–4.

Kobayashi T, Kubo E, Takahashi Y, Kasahara T, Yonezawa H, Akagi Y. Retinal vessel changes in galactose-fed dogs. Arch Ophthalmol Am Med Assoc. 1998;116(6):785–9.

Tso MO, Kurosawa A, Benhamou E, Bauman A, Jeffrey J, Jonasson O. Microangiopathic retinopathy in experimental diabetic monkeys. Trans Am Ophthalmol Soc Am Ophthalmol Soc. 1988;86:389.

Linsenmeier RA, Braun RD, McRipley MA, Padnick LB, Ahmed J, Hatchell DL, et al. Retinal hypoxia in long-term diabetic cats. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 1998;39(9):1647–57.

Jo DH, Cho CS, Kim JH, Jun HO, Kim JH. Animal models of diabetic retinopathy: doors to investigate pathogenesis and potential therapeutics. J Biomed Sci BioMed Central. 2013;20(1):38.

Goldsmith JR, Jobin C. Think small: zebrafish as a model system of human pathology. Biomed Res Int. Hindawi Publishing Corporation; 2012;2012.

Banting FG, Best CH. The internal secretion of the pancreas. Indian J Med Res Indian Counc Med Res. 2007;125(3):L251.

Sirek A. Handbook of diabetes mellitus. Pathophysiology and clinical considerations. Pfeiffer E, Verlag L, editors. Annals of internal medicine. München; 1968. 727–743 p.

Kumar S, Singh R, Vasudeva N, Sharma S. Acute and chronic animal models for the evaluation of anti-diabetic agents. Cardiovasc Diabetol BioMed Central. 2012;11(1):9.

McLetchie NG. Alloxan diabetes: a discovery, albeit a minor one. 2001.

Dixon KC, King AJ, Malinin T. Protein in dying β-cells of the pancreatic islets. Q J Exp Physiol Cogn Med Sci [Internet]. 1960;45(2):202–12. doi:10.1113/expphysiol.1960.sp001458.

Cooperstein S, Watkins D. Alloxan. In The islets of Langerhans. Press A, editor. New York; 1981. 388–411 p.

Rakieten N, Rakieten ML, Nadkarni MV. Studies on the diabetogenic action of streptozotocin (NSC-37917). Cancer Chemother Rep. 1963;29:91–8.

Eleazu CO, Eleazu KC, Chukwuma S, Essien UN. Review of the mechanism of cell death resulting from streptozotocin challenge in experimental animals, its practical use and potential risk to humans. J Diabetes Metab Disord BioMed Central. 2013;12(1):60.

Engerman RL, Kern TS. Experimental galactosemia produces diabetic-like retinopathy. Diabetes Am Diabetes Assoc. 1984;33(1):97–100.

Joussen AM, Doehmen S, Le ML, Koizumi K, Radetzky S, Krohne TU, et al. TNF-α mediated apoptosis plays an important role in the development of early diabetic retinopathy and long-term histopathological alterations. Molecular Vision; 2009.

Stone J, Itin A, Alon T, Pe’Er J, Gnessin H, Chan-Ling T, et al. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci Soc Neurosci. 1995;15(7):4738–47.

Grossniklaus HE, Kang SJ, Berglin L. Animal models of choroidal and retinal neovascularization. Prog Retin Eye Res Elsevier. 2010;29(6):500–19.

Reiser HJ, Whitworth UG Jr, Hatchell DL, Sutherland FS, Nanda S, McAdoo T, et al. Experimental diabetes in cats induced by partial pancreatectomy alone or combined with local injection of alloxan. Lab Anim Sci. 1987;37(4):449–52.

Mansour SZ, Hatchell DL, Chandler D, Saloupis P, Hatchell MC. Reduction of basement membrane thickening in diabetic cat retina by sulindac. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 1990;31(3):457–63.

Hatchell DL, Toth CA, Barden CA, Saloupis P. Diabetic retinopathy in a cat. Exp Eye Res Academic Press. 1995;60(5):591–3.

Jonasson O, Jones CW, Bauman A, John E, Manaligod J, Tso MO, et al. Ann Surg Lippincott, Williams, and Wilkins. 1985;201(1):27.

• Weerasekera LY, Balmer LA, Ram R, Morahan G. Characterization of retinal vascular and neural damage in a novel model of diabetic retinopathy. A novel mouse model of DR. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 2015;56(6):3721–30. Using the recently developed “Collaborative Cross” mouse resource, this study showed for the first time that alloxan-induced DR in mice could manifest in cellular lesions. The creation of mouse strains with high genetic diversity allows for development of new DR models that recapitulate more phenotypes of human disease than were previously possible.

Gaucher D, Chiappore J-A, Pâques M, Simonutti M, Boitard C, Sahel JA, et al. Microglial changes occur without neural cell death in diabetic retinopathy. Vis Res Elsevier. 2007;47(5):612–23.

Kowluru RA, Tang J, Kern TS. Abnormalities of retinal metabolism in diabetes and experimental galactosemia. Diabetes Am Diabetes Assoc. 2001;50(8):1938–42.

Schröder S, Palinski W, Schmid-Schönbein GW. Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy. Am J Pathol Am Soc Investig Pathol. 1991;139(1):81.

Doczi-Keresztesi Z, Jung J, Kiss I, Mezei T, Szabo L, Ember I. Retinal and renal vascular permeability changes caused by stem cell stimulation in alloxan-induced diabetic rats, measured by extravasation of fluorescein. In Vivo (Brooklyn) Int Inst Anticancer Res. 2012;26(3):427–35.

Yang Y, Hayden MR, Sowers S, Bagree SV, Sowers JR. Retinal redox stress and remodeling in cardiometabolic syndrome and diabetes. Oxid Med Cell Longev Hindawi Publishing Corporation. 2010;3(6):392–403.

DiPietro DL, Weinhouse S. Hepatic glucokinase in the fed, fasted, and alloxan-diabetic rat. J Biol Chem ASBMB. 1960;235(9):2542–5.

Crane RK. An effect of alloxan-diabetes on the active transport of sugars by rat small intestine, in vitro. Biochem Biophys Res Commun Elsevier. 1961;4(6):436–40.

Spadella CT, Machado JLM, Lerco MM, Ortolan EVP, Schellini SA, Gregório EA. Temporal relationship between successful pancreas transplantation and control of ocular complications in alloxan-induced diabetic rats. In: Transplantation proceedings. Elsevier; 2008. p. 518–23.

Kern TS, Engerman RL. Comparison of retinal lesions in alloxan-diabetic rats and galactose-fed rats. Curr Eye Res Taylor & Francis. 1994;13(12):863–7.

King JL, Mason JO, Cartner SC, Guidry C. The influence of alloxan-induced diabetes on Müller cell contraction-promoting activities in vitreous. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 2011;52(10):7485–91.

White FR. Streptozotocin. Cancer Chemother Rep. 1963;30:49–53.

Kumar S, Zhuo L. Longitudinal in vivo imaging of retinal gliosis in a diabetic mouse model. Exp Eye Res Elsevier. 2010;91(4):530–6.

Drago F, La Manna C, Emmi I, Marino A. Effects of sulfinpyrazone on retinal damage induced by experimental diabetes mellitus in rabbits. Pharmacol Res Elsevier. 1998;38(2):97–100.

Lee SE, Ma W, Rattigan EM, Aleshin A, Chen L, Johnson LL, et al. Ultrastructural features of retinal capillary basement membrane thickening in diabetic swine. Ultrastruct Pathol Taylor & Francis. 2010;34(1):35–41.

Acharya NK, Qi X, Goldwaser EL, Godsey GA, Wu H, Kosciuk MC, et al.. Retinal pathology is associated with increased blood-retina barrier permeability in a diabetic and hypercholesterolaemic pig model: beneficial effects of the LpPLA2 inhibitor darapladib. Diabetes Vasc Dis Res [Internet]. 2017;1479164116683149. Available from: http://journals.sagepub.com/doi/10.1177/1479164116683149%0A http://www.ncbi.nlm.nih.gov/pubmed/28301218

Li L, Li Y, Zhou Y, Ge Z, Wang L, Li Z, et al. Jiangtang Xiaozhi recipe (降糖消脂方) prevents diabetic retinopathy in streptozotocin-induced diabetic rats. Chin J Integr Med Springer. 2016:1–8.

Anderson HR, Stitt AW, Gardiner TA, Lloyd SJ, Archer DB. Induction of alloxan/streptozotocin diabetes in dogs: a revised experimental technique. Lab Anim SAGE Publications Sage UK: London, England. 1993;27(3):281–5.

Olsen AS, Sarras MP, Intine RV. Limb regeneration is impaired in an adult zebrafish model of diabetes mellitus. Wound repair Regen Wiley Online Library. 2010;18(5):532–42.

Intine RV, Olsen AS, Sarras Jr MP. A zebrafish model of diabetes mellitus and metabolic memory. JoVE J Vis Exp. 2013;(72):e50232–e50232.

Feit-Leichman RA, Kinouchi R, Takeda M, Fan Z, Mohr S, Kern TS, et al. Vascular damage in a mouse model of diabetic retinopathy: relation to neuronal and glial changes. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 2005;46(11):4281–7.

Martin PM, Roon P, Van Ells TK, Ganapathy V, Smith SB. Death of retinal neurons in streptozotocin-induced diabetic mice. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 2004;45(9):3330–6.

Su L, Ji J, Bian J, Fu Y, Ge Y, Yuan Z. Tacrolimus (FK506) prevents early retinal neovascularization in streptozotocin-induced diabetic mice. Int Immunopharmacol Elsevier. 2012;14(4):606–12.

Zhang J, Wu Y, Jin Y, Ji F, Sinclair SH, Luo Y, et al. Intravitreal injection of erythropoietin protects both retinal vascular and neuronal cells in early diabetes. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 2008;49(2):732–42.

Rungger-Brändle E, Dosso AA, Leuenberger PM. Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 2000;41(7):1971–80.

Gardiner TA, Stitt AW, Anderson HR, Archer DB. Selective loss of vascular smooth muscle cells in the retinal microcirculation of diabetic dogs. Br J Ophthalmol BMJ Publishing Group Ltd. 1994;78(1):54–60.

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 Am Assoc Lab Anim Sci. 2002;52(6):523–9.

Kern TS, Engerman RL. A mouse model of diabetic retinopathy. Arch Ophthalmol Am Med Assoc. 1996;114(8):986–90.

Joussen AM, Poulaki V, Le ML, Koizumi K, Esser C, Janicki H, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J FASEB. 2004;18(12):1450–2.

Engerman RL, Kern TS. Retinopathy in animal models of diabetes. Diabetes Metab Res Rev Wiley Online Library. 1995;11(2):109–20.

Helfenstein T, Fonseca FA, Ihara SS, Bottos JM, Moreira FT, Pott H Jr, et al. Impaired glucose tolerance plus hyperlipidaemia induced by diet promotes retina microaneurysms in New Zealand rabbits. Int J Exp Pathol Wiley Online Library. 2011;92(1):40–9.

Gleeson M, Connaughton V, Arneson LS. Induction of hyperglycaemia in zebrafish (Danio rerio) leads to morphological changes in the retina. Acta Diabetol Springer. 2007;44(3):157–63.

Hyoung Kim J, Suk Yu Y, Kim K, Hun KJ. Investigation of barrier characteristics in the hyaloid-retinal vessel of zebrafish. J Neurosci Res Wiley Online Library. 2011;89(6):921–8.

Cusick M, Chew EY, Ferris F, Cox TA, Chan C-C, Kador PF. Effects of aldose reductase inhibitors and galactose withdrawal on fluorescein angiographic lesions in galactose-fed dogs. Arch Ophthalmol Am Med Assoc. 2003;121(12):1745–51.

Dollery CT, Bulpitt CJ, Kohner EM. Oxygen supply to the retina from the retinal and choroidal circulations at normal and increased arterial oxygen tensions. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 1969;8(6):588–94.

Aiello LP, Pierce EA, Foley ED, Takagi H, Chen H, Riddle L, et al. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci U S A [Internet]. 1995;92(23):10457–61. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=40630&tool=pmcentrez&rendertype=abstract.

Chen X, Ouyang L, Yin Z, Xia Y, Chen X, Shi H, et al. Effects of microRNA-29a on retinopathy of prematurity by targeting AGT in a mouse model. Am J Transl Res. 2017;9(2):791–801.

Zhang P, Wang H, Cao H, Xu X, Sun T. Insulin-like growth factor binding protein-related protein 1 inhibit retinal neovascularization in the mouse model of oxygen-induced retinopathy. J Ocul Pharmacol Ther. Mary Ann Liebert, Inc. 140 Huguenot Street, 3rd Floor New Rochelle, NY 10801 USA; 2017.

van Wijngaarden P, Coster DJ, Brereton HM, Gibbins IL, Williams KA. Strain-dependent differences in oxygen-induced retinopathy in the inbred rat. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 2005;46(4):1445–52.

Penn JS, Henry MM, Tolman BL. Exposure to alternating hypoxia and hyperoxia causes severe proliferative retinopathy in the newborn rat. Pediatr Res Nature Publishing Group. 1994;36(6):724–31.

Downie LE, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL, Fletcher EL. AT1 receptor inhibition prevents astrocyte degeneration and restores vascular growth in oxygen-induced retinopathy. Glia Wiley Online Library. 2008;56(10):1076–90.

Downie LE, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL, Fletcher EL. Neuronal and glial cell changes are determined by retinal vascularization in retinopathy of prematurity. J Comp Neurol Wiley Online Library. 2007;504(4):404–17.

Fulton AB, Reynaud X, Hansen RM, Lemere CA, Parker C, Williams TP. Rod photoreceptors in infant rats with a history of oxygen exposure. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 1999;40(1):168–74.

Cao Z, Jensen LD, Rouhi P, Hosaka K, Länne T, Steffensen JF, et al. Hypoxia-induced retinopathy model in adult zebrafish. Nat Protoc Nature Publishing Group. 2010;5(12):1903–10.

Cao R, Jensen LDE, Söll I, Hauptmann G, Cao Y. Hypoxia-induced retinal angiogenesis in zebrafish as a model to study retinopathy. PLoS One Public Library of Science. 2008;3(7):e2748.

Miller JW, Adamis AP, Shima DT, D’Amore PA, Moulton RS, O’Reilly MS, et al. Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am J Pathol. 1994;145(3):574–84.

Liu G, Zhang W, Xiao Y, Lu P. Critical role of IP-10 on reducing experimental corneal neovascularization. CurrEye Res. 2014;3683(1460–2202 (Electronic)):1–11.

Weir GC, Marselli L, Marchetti P, Katsuta H, Jung MH, Bonner-Weir S. Towards better understanding of the contributions of overwork and glucotoxicity to the β-cell inadequacy of type 2 diabetes. Diabetes Obes Metab Wiley Online Library. 2009;11(s4):82–90.

Wang J, Takeuchi T, Tanaka S, Kubo S-K, Kayo T, Lu D, et al. A mutation in the insulin 2 gene induces diabetes with severe pancreatic β-cell dysfunction in the Mody mouse. J Clin Invest [Internet] Am Soc Clin Investig. 1999;103(1):27–37. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC407861/.

Izumi T, Yokota-Hashimoto H, Zhao S, Wang J, Halban PA, Takeuchi T. Dominant negative pathogenesis by mutant proinsulin in the Akita diabetic mouse. Diabetes [Internet]. 2003;52(2):409 LP–416. Available from: http://diabetes.diabetesjournals.org/content/52/2/409.abstract.

Barber AJ, Antonetti DA, Kern TS, Reiter CEN, Soans RS, Krady JK, et al. The Ins2Akita mouse as a model of early retinal complications in diabetes. Invest Ophthalmol Vis Sci [Internet]. 2005;46(6):2210–8. doi:10.1167/iovs.04-1340.

Han Z, Guo J, Conley SM, Naash MI. Retinal angiogenesis in the Ins2(Akita) mouse model of diabetic retinopathy. Invest Ophthalmol Vis Sci [Internet] Assoc Res Vis Ophthalmol. 2013;54(1):574–84. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3558298/.

Gastinger MJ, Singh RSJ, Barber AJ. Loss of cholinergic and dopaminergic amacrine cells in streptozotocin-diabetic rat and Ins2Akita-diabetic mouse retinas. Invest Ophthalmol Vis Sci [Internet]. 2006;47(7):3143–50. doi:10.1167/iovs.05-1376.

Gastinger MJ, Kunselman AR, Conboy EE, Bronson SK, Barber AJ. Dendrite remodeling and other abnormalities in the retinal ganglion cells of Ins2Akita diabetic mice. Invest Ophthalmol Vis Sci [Internet]. 2008;49(6):2635–42. doi:10.1167/iovs.07-0683.

Leiter EH. The NOD mouse: a model for analyzing the interplay between heredity and environment in development of autoimmune disease. ILAR J [Internet]. 1993 Jan 1;35(1):4–14. doi:10.1093/ilar.35.1.4.

Serreze DV, Chapman HD, Varnum DS, Gerling I, Leiter EH, Shultz LD. Initiation of autoimmune diabetes in NOD/Lt mice is MHC class I-dependent. J Immunol [Internet]. 1997;158(8):3978 LP–3986. http://www.jimmunol.org/content/158/8/3978.abstract.

Baxter AG, Cooke A. The genetics of the NOD mouse. Diabetes Metab Rev [Internet] Wiley. 1995;11(4):315–35. doi:10.1002/dmr.5610110403.

Leiter EH, Prochazka M, Coleman DL. The non-obese diabetic (NOD) mouse. Am J Pathol Am Soc Investig Pathol. 1987;128(2):380.

Simpson PB, Mistry MS, Maki RA, Yang W, Schwarz DA, Johnson EB, et al. Cutting edge: diabetes-associated quantitative trait locus, Idd4, is responsible for the IL-12p40 overexpression defect in nonobese diabetic (NOD) mice. J Immunol Am Assoc Immnol. 2003;171(7):3333–7.

Li C-R, Sun S-G. VEGF expression and cell apoptosis in NOD mouse retina. Int J Ophthalmol [Internet] Int J Ophthalmol Press. 2010;3(3):224–7. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3340636/.

Shaw SG, Boden JP, Biecker E, Reichen J, Rothen B. Endothelin antagonism prevents diabetic retinopathy in NOD mice: a potential role of the angiogenic factor adrenomedullin. Exp Biol Med SAGE Publications. 2006;231(6):1101–5.

Lee S, Harris NR. Losartan and ozagrel reverse retinal arteriolar constriction in non-obese diabetic mice. Microcirculation [Internet]. 2008;15(5):379–87. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2527598/.

Faulds MH, Zhao C, Dahlman-Wright K, Gustafsson J-Å. The diversity of sex steroid action: regulation of metabolism by estrogen signaling. J Endocrinol [Internet]. 2012;212(1):3–12. Available from: http://joe.endocrinology-journals.org/content/212/1/3.abstract.

Yoon J-W, Leiter EH, Coleman DL, Kim MK, Pak CY, McArthur RG, et al. Genetic control of organ-reactive autoantibody production in mice by obesity (ob) diabetes (db) genes. Diabetes [Internet]. 1988;37(9):1287 LP–1293. Available from: http://diabetes.diabetesjournals.org/content/37/9/1287.abstract.

Leiter EH, Coleman DL, Eppig JJ. Endocrine pancreatic cells of postatal “diabetes” (DB) mice in cell culture. In Vitro Springer. 1979;15(7):507–21.

Tang L, Zhang Y, Jiang Y, Willard L, Ortiz E, Wark L, et al. Dietary wolfberry ameliorates retinal structure abnormalities in db/db mice at the early stage of diabetes. Exp Biol Med SAGE Publications Sage UK: London, England. 2011;236(9):1051–63.

Clements RS, Robison WG, Cohen MP. Anti-glycated albumin therapy ameliorates early retinal microvascular pathology in db/db mice. J Diabetes Complicat Elsevier. 1998;12(1):28–33.

Cheung AKH, Fung MKL, Lo ACY, Lam TTL, So KF, Chung SSM, et al. Aldose reductase deficiency prevents diabetes-induced blood-retinal barrier breakdown, apoptosis, and glial reactivation in the retina of db/db mice. Diabetes Am Diabetes Assoc. 2005;54(11):3119–25.

Belke DD, Larsen TS, Gibbs EM, Severson DL. Altered metabolism causes cardiac dysfunction in perfused hearts from diabetic (db/db) mice. Am J Physiol Metab Am Physiol Soc. 2000;279(5):E1104–13.

Aasum E, Hafstad AD, Severson DL, Larsen TS. Age-dependent changes in metabolism, contractile function, and ischemic sensitivity in hearts from db/db mice. Diabetes Am Diabetes Assoc. 2003;52(2):434–41.

Okamoto N, Tobe T, Hackett SF, Ozaki H, Vinores MA, LaRochelle W, et al. Transgenic mice with increased expression of vascular endothelial growth factor in the retina: a new model of intraretinal and subretinal neovascularization. Am J Pathol Am Soc Investig Pathol. 1997;151(1):281.

Tee LBG, Penrose MA, O’Shea JE, Lai CM, Rakoczy EP, Dunlop SA. VEGF-induced choroidal damage in a murine model of retinal neovascularisation. Br J Ophthalmol BMJ Publishing Group Ltd. 2008;92(6):832–8.

van Eeden PE, LBG T, Lukehurst S, Lai C-M, Rakoczy EP, Beazley LD, et al. Early vascular and neuronal changes in a VEGF transgenic mouse model of retinal neovascularization. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 2006;47(10):4638–45.

Shen W-Y, Lai CM, Graham CE, Binz N, Lai YKY, Eade J, et al. Long-term global retinal microvascular changes in a transgenic vascular endothelial growth factor mouse model. Diabetologia Springer. 2006;49(7):1690–701.

Rakoczy EP, Rahman ISA, Binz N, Li C-R, Vagaja NN, de Pinho M, et al. Characterization of a mouse model of hyperglycemia and retinal neovascularization. Am J Pathol Elsevier. 2010;177(5):2659–70.

McLenachan S, Magno AL, Ramos D, Catita J, McMenamin PG, Chen FK, et al. Angiography reveals novel features of the retinal vasculature in healthy and diabetic mice. Exp Eye Res Elsevier. 2015;138:6–21.

Wisniewska-Kruk J, Klaassen I, Vogels IMC, Magno AL, Lai C-M, Van Noorden CJF, et al. Molecular analysis of blood–retinal barrier loss in the Akimba mouse, a model of advanced diabetic retinopathy. Exp Eye Res Elsevier. 2014;122:123–31.

Schmidt RE, Dorsey DA, Beaudet LN, Peterson RG. Analysis of the Zucker diabetic fatty (ZDF) type 2 diabetic rat model suggests a neurotrophic role for insulin/IGF-I in diabetic autonomic neuropathy. Am J Pathol Elsevier. 2003;163(1):21–8.

Seino S. A novel rat model of type 2 diabetes: the Zucker fatty diabetes mellitus ZFDM rat. Exp Diabetes Res Hindawi Publishing Corporation. 2013;2013

Danis RP, Yang Y. Microvascular retinopathy in the Zucker diabetic fatty rat. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 1993;34(7):2367–71.

Watanabe TK, Suzuki M, Yamasaki Y, Okuno S, Hishigaki H, Ono T, et al. Mutated G-protein-coupled receptor GPR10 is responsible for the hyperphagia/dyslipidaemia/obesity locus of Dmo1 in the OLETF Rat. Clin Exp Pharmacol Physiol Wiley Online Library. 2005;32(5–6):355–66.

Lu Z-Y, Bhutto IA, Amemiya T. Retinal changes in Otsuka Long-Evans Tokushima fatty rats (spontaneously diabetic rat)—possibility of a new experimental model for diabetic retinopathy. Jpn J Ophthalmol Elsevier. 2003;47(1):28–35.

Miyamura N, Bhutto IA, Amemiya T. Retinal capillary changes in Otsuka Long-Evans Tokushima fatty rats (spontaneously diabetic strain). Ophthalmic Res Karger Publishers. 1999;31(5):358–66.

Bhutto IA, Lu Z-Y, Takami Y, Amemiya T. Retinal and choroidal vasculature in rats with spontaneous diabetes type 2 treated with the angiotensin-converting enzyme inhibitor cilazapril: corrosion cast and electron-microscopic study. Ophthalmic Res Karger Publishers. 2002;34(4):220–31.

Sima AAF, Chakrabarti S, Garcia-Salinas R, Basu PK. The BB-rat—an authentic model of human diabetic retinopathy. Curr Eye Res Taylor & Francis. 1985;4(10):1087–92.

Wallis RH, Wang K, Marandi L, Hsieh E, Ning T, Chao GYC, et al. Type 1 diabetes in the BB rat: a polygenic disease. Diabetes Am Diabetes Assoc. 2009;58(4):1007–17.

MacMurray AJ, Moralejo DH, Kwitek AE, Rutledge EA, Van Yserloo B, Gohlke P, et al. Lymphopenia in the BB rat model of type 1 diabetes is due to a mutation in a novel immune-associated nucleotide (Ian)-related gene. Genome Res Cold Spring Harbor Lab. 2002;12(7):1029–39.

Hornum L, Rømer J, Markholst H. The diabetes-prone BB rat carries a frameshift mutation in Ian4, a positional candidate of Iddm1. Diabetes Am Diabetes Assoc. 2002;51(6):1972–9.

Rutledge EA, Fuller JM, Van Yserloo B, Moralejo DH, Ettinger RA, Gaur P, et al. Sequence variation and expression of the Gimap gene family in the BB rat. Exp Diabetes Res Hindawi Publishing Corporation. 2009;2009

Ash S, Yarkoni S, Askenasy N. Lymphopenia is detrimental to therapeutic approaches to type 1 diabetes using regulatory T cells. Immunol Res Springer. 2014;58(1):101–5.

von Känel R, Mills PJ, Dimsdale JE. Short-term hyperglycemia induces lymphopenia and lymphocyte subset redistribution. Life Sci Elsevier. 2001;69(3):255–62.

Ray-Coquard I, Cropet C, Van Glabbeke M, Sebban C, Le Cesne A, Judson I, et al. Lymphopenia as a prognostic factor for overall survival in advanced carcinomas, sarcomas, and lymphomas. Cancer Res AACR. 2009;69(13):5383–91.

Grossman SA, Ellsworth S, Campian J, Wild AT, Herman JM, Laheru D, et al. Survival in patients with severe lymphopenia following treatment with radiation and chemotherapy for newly diagnosed solid tumors. J Natl Compr Cancer Netw. Harborside press, LLC; 2015;13(10):1225–1231.

Schulze-Koops H. Lymphopenia and autoimmune diseases. Arthritis Res Ther BioMed Central. 2004;6(4):178.

Miyamura N, Amemiya T. Lens and retinal changes in the WBN/Kob rat (spontaneously diabetic strain). Ophthalmic Res Karger Publishers. 1998;30(4):221–32.

Tsuji N, Matsuura T, Ozaki K, Tomoya S, Narama I. Diabetic retinopathy and choroidal angiopathy in diabetic rats (WBN/Kob). Exp Anim. Japanese Association for Laboratory Animal Science; 2009;58(5):481–7.

Tsuji A, Nishikawa T, Mori M, Suda K, Nishimori I, Nishimura M. Quantitative trait locus analysis for chronic pancreatitis and diabetes mellitus in the WBN/Kob rat. Genomics Elsevier. 2001;74(3):365–9.

Xiaoying FU, Lei C, Zhang G, Higuchi K. Hereditary pancreatitis model WBN/Kob rat strain has a unique haplotype in the Pdwk1 region on chromosome 7. Exp Anim Japanese Assoc Lab Anim Sci. 2009;58(4):409–13.

Yamada H, Yamada E, Higuchi A, Matsumura M. Retinal neovascularisation without ischaemia in the spontaneously diabetic Torii rat. Diabetologia. Springer. 2005;48(8):1663–8.

Shinohara M, Masuyama T, Shoda T, Takahashi T, Katsuda Y, Komeda K, et al. A new spontaneously diabetic non-obese Torii rat strain with severe ocular complications. J Diabetes Res Hindawi Publishing Corporation. 2000;1(2):89–100.

Sasase T, Morinaga H, Abe T, Miyajima K, Ohta T, Shinohara M, et al. Protein kinase C beta inhibitor prevents diabetic peripheral neuropathy, but not histopathological abnormalities of retina in spontaneously diabetic Torii rat. Diabetes Obes Metab Wiley Online Library. 2009;(11):11, 1084–1017.

Matsuoka M, Ogata N, Minamino K, Matsumura M. Leukostasis and pigment epithelium-derived factor in rat models of diabetic retinopathy. Mol Vis Citeseer. 2007;13:1058–65.

Fukuda M, Nakanishi Y, Fuse M, Yokoi N, Hamada Y, Fukagawa M, et al. Altered expression of aquaporins 1 and 4 coincides with neurodegenerative events in retinas of spontaneously diabetic Torii rats. Exp Eye Res Elsevier. 2010;90(1):17–25.

Kakehashi A, Saito Y, Mori K, Sugi N, Ono R, Yamagami H, et al. Characteristics of diabetic retinopathy in SDT rats. Diabetes Metab Res Rev Wiley Online Library. 2006;22(6):455–61.

Masuyama T, Fuse M, Yokoi N, Shinohara M, Tsujii H, Kanazawa M, et al. Genetic analysis for diabetes in a new rat model of nonobese type 2 diabetes, spontaneously diabetic Torii rat. Biochem Biophys Res Commun Elsevier. 2003;304(1):196–206.

Goto Y, Suzuki K, Ono T, Sasaki M, Toyota T. Development of diabetes in the non-obese NIDDM rat (GK rat). In: Prediabetes. Springer; 1988. p. 29–31.

Agardh C-D, Agardh E, Zhang H, Östenson C-G. Altered endothelial/pericyte ratio in Goto-Kakizaki rat retina. J Diabetes Complications Elsevier. 1997;11(3):158–62.

Miyamoto K, Ogura Y, Nishiwaki H, Matsuda N, Honda Y, Kato S, et al. Evaluation of retinal microcirculatory alterations in the Goto-Kakizaki rat. A spontaneous model of non-insulin-dependent diabetes. Invest Ophthalmol Vis Sci Assoc Res Vis Ophthalmol. 1996;37(5):898–905.

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 Elsevier. 2000;4(6):590–6.

Kakizaki M, Masaki N. Spontaneous diabetes produced by selective breeding of normal Wistar rats. Proc Jpn Acad The Japan Academy. 1975;51(1):80–5.

Liu T, Li H, Ding G, Wang Z, Chen Y, Liu L, et al. Comparative genome of GK and Wistar rats reveals genetic basis of type 2 diabetes. PLoS One Public Library of Science. 2015;10(11):e0141859.

van Rooijen E, Voest EE, Logister I, Bussmann J, Korving J, van Eeden FJ, et al. von Hippel-Lindau tumor suppressor mutants faithfully model pathological hypoxia-driven angiogenesis and vascular retinopathies in zebrafish. Dis Model Mech [Internet]. 2010;3(5–6):343 LP–353. Available from: http://dmm.biologists.org/content/3/5-6/343.abstract.

Krämer A, Green J, Pollard J, Tugendreich S. Causal analysis approaches in ingenuity pathway analysis. Bioinformatics [Internet] Oxford University Press. 2014;30(4):523–30. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3928520/.

Thông tin
Thông tin xuất bản

Current Diabetes Reports

Tập 17

1-17

Thông tin tác giả