Advanced glycation end-products stimulate basic fibroblast growth factor expression in cultured Müller cells

Ai,Jing; Liu,Yao; Sun,Jun-Hui

doi:10.3892/mmr.2012.1152

Advanced glycation end-products stimulate basic fibroblast growth factor expression in cultured Müller cells

Authors:
- Jing Ai
- Yao Liu
- Jun-Hui Sun
View Affiliations

Affiliations: Department of Ophthalmology, Second Affiliated Hospital (Binjiang Branch), School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310009, P.R. China, Department of Ophthalmology, Zhongda Hospital, Southeast University, Nanjing, Jiangsu 210009, P.R. China, Key Laboratory of Combined Multi-organ Transplantation, Ministry of Public Health, First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310003, P.R. China
Published online on: October 24, 2012 https://doi.org/10.3892/mmr.2012.1152
Pages: 16-20
Copyright: © Ai et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Accumulating evidence points to a causal role for advanced glycation end-products (AGEs) in the development of diabetic vascular complications, including diabetic retinopathy (DR). To assess the reciprocal correlation between AGEs and basic fibroblast growth factor (bFGF), the effects of AGEs on the production of bFGF by Müller cells were investigated. Müller cells were cultured from adult rabbit retinas. The AGEs were prepared with highly glycated bovine serum albumin (BSA) and the control non‑glycated BSA (BSA control) was incubated under the same conditions without glucose. Cultured Müller cells were exposed to AGEs or BSA control (volume percentages were 4, 8, 16, 32 and 64%) for a time course of 1, 3, 6 and 9 days in their desired medium. The expression of bFGF in Müller cells was evaluated by immunocytochemistry. Quantification was performed by densitometry using computerized image analysis with dedicated software. AGEs in a volume percentage of 16 and 32% on day 1 and in a volume percentage of 16, 32 and 64% on days 3, 6 and 9 increased the bFGF expression in Müller cells (P<0.05). Additionally, AGEs upregulated bFGF expression in Müller cells in a time‑dependent manner. In conclusion, the treatment of Müller cells with AGEs resulted in a dose- and time‑dependent elevation of bFGF in the culture medium. The results from this study suggest that the increased formation of AGEs in the vitreous may be involved in the development of DR by inducing the production of bFGF by retinal Müller cells.

View Figures

View References

1	Daroux M, Prévost G, Maillard-Lefebvre H, Gaxatte C, D’Agati VD, Schmidt AM and Boulanger E: Advanced glycation end-products: implications for diabetic and non-diabetic nephropathies. Diabetes Metab. 36:1–10. 2010. View Article : Google Scholar : PubMed/NCBI
2	Berrou J, Tostivint I, Verrecchia F, Berthier C, Boulanger E, Mauviel A, Marti HP, Wautier MP, Wautier JL, Rondeau E and Hertig A: Advanced glycation end products regulate extracellular matrix protein and protease expression by human glomerular mesangial cells. Int J Mol Med. 23:513–520. 2009.
3	Wolffenbuttel BH, Giordano D, Founds HW and Bucala R: Long-term assessment of glucose control by haemoglobin-AGE measurement. Lancet. 347:513–515. 1996. View Article : Google Scholar : PubMed/NCBI
4	Meerwaldt R, Links T, Zeebregts C, Tio R, Hillebrands JL and Smit A: The clinical relevance of assessing advanced glycation endproducts accumulation in diabetes. Cardiovasc Diabetol. 7:292008. View Article : Google Scholar : PubMed/NCBI
5	Yamagishi S: Role of advanced glycation end products (AGEs) and receptor for AGEs (RAGE) in vascular damage in diabetes. Exp Gerontol. 46:217–224. 2011. View Article : Google Scholar : PubMed/NCBI
6	Bringmann A and Wiedemann P: Involvement of Müller glial cells in epiretinal membrane formation. Graefes Arch Clin Exp Ophthalmol. 247:865–883. 2009.
7	Simó R, Carrasco E, García-Ramírez M and Hernández C: Angiogenic and antiangiogenic factors in proliferative diabetic retinopathy. Curr Diabetes Rev. 2:71–98. 2006.
8	Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR, Thieme H, Iwamoto MA, Park JE, et al: Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 331:1480–1487. 1994. View Article : Google Scholar : PubMed/NCBI
9	Kakehashi A, Inoda S, Mameuda C, Kuroki M, Jono T, Nagai R, Horiuchi S, Kawakami M and Kanazawa Y: Relationship among VEGF, VEGF receptor, AGEs and macrophages in proliferative diabetic retinopathy. Diabetes Res Clin Pract. 79:438–445. 2008. View Article : Google Scholar : PubMed/NCBI
10	Payne JF, Tangpricha V, Cleveland J, Lynn MJ, Ray R and Srivastava SK: Serum insulin-like growth factor-I in diabetic retinopathy. Mol Vis. 17:2318–2324. 2011.PubMed/NCBI
11	Shimizu F, Sano Y, Haruki H and Kanda T: Advanced glycation end-products induce basement membrane hypertrophy in endoneurial microvessels and disrupt the blood-nerve barrier by stimulating the release of TGF-β and vascular endothelial growth factor (VEGF) by pericytes. Diabetologia. 54:1517–1526. 2011.PubMed/NCBI
12	Simó R, Vidal MT, García-Arumí J, Carrasco E, García-Ramírez M, Segura RM and Hernández C: Intravitreous hepatocyte growth factor in patients with proliferative diabetic retinopathy: a case-control study. Diabetes Res Clin Pract. 71:36–44. 2006.
13	Yang XM, Yafai Y, Wiedemann P, Kuhrt H, Wang YS, Reichenbach A and Eichler W: Hypoxia-induced upregulation of pigment epithelium-derived factor by retinal glial (Müller) cells. J Neurosci Res. 90:257–266. 2012.PubMed/NCBI
14	He S, Jin ML, Worpel V and Hinton DR: A role for connective tissue growth factor in the pathogenesis of choroidal neovascularization. Arch Ophthalmol. 121:1283–1288. 2003. View Article : Google Scholar : PubMed/NCBI
15	Watanabe D, Suzuma K, Suzuma I, Ohashi H, Ojima T, Kurimoto M, Murakami T, Kimura T and Takagi H: Vitreous levels of angiopoietin 2 and vascular endothelial growth factor in patients with proliferative diabetic retinopathy. Am J Ophthalmol. 139:476–481. 2005. View Article : Google Scholar : PubMed/NCBI
16	Cao R, Eriksson A, Kubo H, Alitalo K, Cao Y and Thyberg J: Comparative evaluation of FGF-2-, VEGF-A- and VEGF-C-induced angiogenesis, lymphangiogenesis, vascular fenestrations and permeability. Circ Res. 94:664–670. 2004. View Article : Google Scholar : PubMed/NCBI
17	Tokuda H, Adachi S, Matsushima-Nishiwaki R, Kato K, Natsume H, Otsuka T and Kozawa O: Enhancement of basic fibroblast growth factor-stimulated VEGF synthesis by Wnt3a in osteoblasts. Int J Mol Med. 27:859–864. 2011. View Article : Google Scholar : PubMed/NCBI
18	Lee JJ, Hsiao CC, Yang IH, Chou MH, Wu CL, Wei YC, Chen CH and Chuang JH: High-mobility group box 1 protein is implicated in advanced glycation end products-induced vascular endothelial growth factor A production in the rat retinal ganglion cell line RGC-5. Mol Vis. 18:838–850. 2012.PubMed/NCBI
19	Wakakura M and Foulds WS: Immunocytochemical characteristics of Müller cells cultured from adult rabbit retina. Invest Ophthalmol Vis Sci. 29:892–900. 1988.
20	Liu Y and Wakakura M: P1-/P2-purinergic receptors on cultured rabbit retinal Müller cells. Jpn J Ophthalmol. 42:33–40. 1998.
21	Neumann A, Schinzel R, Palm D, Riederer P and Münch G: High molecular weight hyaluronic acid inhibits advanced glycation endproduct-induced NF-kappaB activation and cytokine expression. FEBS Lett. 453:283–287. 1999. View Article : Google Scholar : PubMed/NCBI
22	Vlassara H, Brownlee M, Manogue KR, Dinarello CA and Pasagian A: Cachectin/TNF and IL-1 induced by glucose-modified proteins: role in normal tissue remodeling. Science. 240:1546–1548. 1988. View Article : Google Scholar
23	Walcher D and Marx N: Advanced glycation end products and C-peptide-modulators in diabetic vasculopathy and atherogenesis. Semin Immunopathol. 31:103–111. 2009. View Article : Google Scholar : PubMed/NCBI
24	Yamagishi S, Maeda S, Matsui T, Ueda S, Fukami K and Okuda S: Role of advanced glycation end products (AGEs) and oxidative stress in vascular complications in diabetes. Biochim Biophys Acta. 1820:663–671. 2012. View Article : Google Scholar : PubMed/NCBI
25	Nam MH, Lee HS, Seomun Y, Lee Y and Lee KW: Monocyte-endothelium-smooth muscle cell interaction in co-culture: proliferation and cytokine productions in response to advanced glycation end products. Biochim Biophys Acta. 1810:907–912. 2011. View Article : Google Scholar : PubMed/NCBI
26	Curtis TM, Hamilton R, Yong PH, McVicar CM, Berner A, Pringle R, Uchida K, Nagai R, Brockbank S and Stitt AW: Müller glial dysfunction during diabetic retinopathy in rats is linked to accumulation of advanced glycation end-products and advanced lipoxidation end-products. Diabetologia. 54:690–698. 2011.
27	Bhatia B, Jayaram H, Singhal S, Jones MF and Limb GA: Differences between the neurogenic and proliferative abilities of Müller glia with stem cell characteristics and the ciliary epithelium from the adult human eye. Exp Eye Res. 93:852–861. 2011.PubMed/NCBI
28	Guidry C, King JL and Mason JO III: Fibrocontractive Müller cell phenotypes in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci. 50:1929–1939. 2009.PubMed/NCBI
29	King JL, Mason JO III, Cartner SC and Guidry C: The influence of alloxan-induced diabetes on Müller cell contraction-promoting activities in vitreous. Invest Ophthalmol Vis Sci. 52:7485–7491. 2011.
30	Crawford TN, Alfaro DV III, Kerrison JB and Jablon EP: Diabetic retinopathy and angiogenesis. Curr Diabetes Rev. 5:8–13. 2009. View Article : Google Scholar
31	Liu W, Xu J, Wang M, Wang Q, Bi Y and Han M: Tumor-derived vascular endothelial growth factor (VEGF)-a facilitates tumor metastasis through the VEGF-VEGFR1 signaling pathway. Int J Oncol. 39:1213–1220. 2011.PubMed/NCBI
32	Dieudonné SC, La Heij EC, Diederen RM, Kessels AG, Liem AT, Kijlstra A and Hendrikse F: Balance of vascular endothelial growth factor and pigment epithelial growth factor prior to development of proliferative vitreoretinopathy. Ophthalmic Res. 39:148–154. 2007.PubMed/NCBI
33	Funatsu H, Noma H, Mimura T, Eguchi S and Hori S: Association of vitreous inflammatory factors with diabetic macular edema. Ophthalmology. 116:73–79. 2009. View Article : Google Scholar : PubMed/NCBI
34	Baharivand N, Zarghami N, Panahi F, Dokht Ghafari MY, Mahdavi Fard A and Mohajeri A: Relationship between vitreous and serum vascular endothelial growth factor levels, control of diabetes and microalbuminuria in proliferative diabetic retinopathy. Clin Ophthalmol. 6:185–191. 2012.
35	Kanda S, Naba A and Miyata Y: Inhibition of endothelial cell chemotaxis toward FGF-2 by gefitinib associates with downregulation of Fes activity. Int J Oncol. 35:1305–1312. 2009. View Article : Google Scholar : PubMed/NCBI
36	Hollborn M, Jahn K, Limb GA, Kohen L, Wiedemann P and Bringmann A: Characterization of the basic fibroblast growth factor-evoked proliferation of the human Müller cell line, MIO-M1. Graefes Arch Clin Exp Ophthalmol. 242:414–422. 2004.PubMed/NCBI
37	Zakareia FA, Alderees AA, Al Regaiy KA and Alrouq FA: Correlation of electroretinography b-wave absolute latency, plasma levels of human basic fibroblast growth factor, vascular endothelial growth factor, soluble fatty acid synthase and adrenomedullin in diabetic retinopathy. J Diabetes Complications. 24:179–185. 2010. View Article : Google Scholar
38	Matsui M and Tabata Y: Enhanced angiogenesis by multiple release of platelet-rich plasma contents and basic fibroblast growth factor from gelatin hydrogels. Acta Biomater. 8:1792–1801. 2012. View Article : Google Scholar : PubMed/NCBI
39	Gündüz K and Bakri SJ: Management of proliferative diabetic retinopathy. Compr Ophthalmol Update. 8:245–256. 2007.