Relationship between adiponectin and diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Li Yunyun ,  Liu Ningpu

Beijing Ophthalmology and Visual Sciences Key Laboratory, Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University, Beijing 100730, China;

Corresponding author：

Liu Ningpu, Email: nliu001@gmail.com

Keywords：

Diabetic retinopathy/etiology; Adiponectin; Review

DOI：

10.3760/cma.j.issn.1005-1015.2017.03.029

Video：

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The exact pathophysiological mechanisms of diabetic retinopathy (DR) remain elusive. The inflammatory reaction, retinal vascular leakage and retinal neovascularization are main features of DR. Adiponectin (APN) is an endogenous biological active protein secreted by adipocytes. It can increase insulin sensitivity, regulate blood glucose and lipid metabolism, and has anti-inflammation and anti-neovascularization functions. It may be involved in the development of DR. This review summarized the studies on the association between APN and DR in recent years.

Citation： Li Yunyun, Liu Ningpu. Relationship between adiponectin and diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2017, 33(3): 324-327. doi: 10.3760/cma.j.issn.1005-1015.2017.03.029 Copy

1.	Kern PA, Di Gregorio GB,Lu T, et al. Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression[J]. Diabetes, 2003, 52(7): 1779-1785.
2.	Lee B, Shao J.Adiponectin and energy homeostasis [J]. Rev Endocr Metab Disord, 2014, 15(2): 149-156. DOI: 10.1007/s11154-013-9283-3.
3.	Ohashi K, Ouchi N, Matsuzawa Y. Anti-inflammatory and anti-atherogenic properties of adiponectin [J]. Biochimie, 2012, 94(10): 2137-2142. DOI: 10.1016/j.biochi.2012.06.008.
4.	Krenning G, Moonen JR, Harmsen MC. Pleiotropism of adiponectin: inflammation, neovascularization, and fibrosis [J]. Circ Res, 2009, 104(9): 1029-1031. DOI: 10.1161/CIRCRESAHA.109.198044.
5.	Kobayashi H, Ouchi N, Kihara S, et al. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin [J]. Circ Res, 2004, 94(4): 27-31. DOI: 10.1161/01.RES.0000119921.86460.37.
6.	Yilmaz MI, Sonmez A, Acikel C, et al. Adiponectin may play a part in the pathogenesis of diabetic retinopathy[J]. Eur J Endocrinol, 2004, 151(1): 135-140.
7.	Kato K, Osawa H, Ochi M, et al. Serum total and high molecular weight adiponectin levels are correlated with the severity of diabetic retinopathy and nephropathy [J]. Clin Endocrinol (Oxf), 2008, 68(3): 442-449. DOI: 10.1111/j.1365-2265.2007.03063.x.
8.	Kuo JZ, Guo X, Klein R, et al. Adiponectin, insulin sensitivity and diabetic retinopathy in latinos with type 2 diabetes [J]. J Clin Endocrinol Metab, 2015, 100(9): 3348-3355. DOI: 10.1210/jc.2015-1221.
9.	Pradeepa R, Surendar J, Indulekha K, et al. Association of serum adiponectin with diabetic microvascular complications among south Indian type 2 diabetic subjects - (CURES-133)[J]. Clin Biochem, 2015, 48(1-2): 33-38. DOI: 10.1016/j.clinbiochem.2014.10.009.
10.	Matsuda M, Kawasaki F, Yamada K, et al. Impact of adiposity and plasma adipocytokines on diabetic angiopathies in Japanese type 2 diabetic subjects[J]. Diabet Med, 2004, 21(8): 881-888. DOI: 10.1111/j.1464-5491.2004.01261.x.
11.	Vionnet N, Hani EH, Dupont S,et al. Genomewide search for type 2 diabetes-susceptibility genes in French whites: evidence for a novel susceptibility locus for early-onset diabetes on chromosome 3q27-qter and independent replication of a type 2-diabetes locus on chromosome 1q21-q24[J]. Am J Hum Genet, 2000, 67(6): 1470-1480.
12.	Calton EK, Miller VS, Soares MJ.Factors determining the risk of the metabolic syndrome: is there a central role for adiponectin?[J]. Eur J Clin Nutr, 2013, 67(5): 485-491. DOI: 10.1038/ejcn.2013.1.
13.	Kadowaki T, Yamauchi T.Adiponectin and adiponectin receptors[J]. Endocr Rev, 2005, 26(3): 439-451. DOI: 10.1210/er.2005-0005.
14.	Lin T, Qiu Y, Liu Y,et al. Expression of adiponectin and its receptors in type 1 diabetes mellitus in human and mouse retinas[J]. Mol Vis, 2013, 19: 1769-1778.
15.	Hsu YJ, Wang LC, Yang WS, et al. Effects of fenofibrate on adiponectin expression in retinas of streptozotocin-induced diabetic rats[J/OL].J Diabetes Res, 2014, 2014: 540326 [2014-12-01]. . DOI: 10.1155/2014/540326.
16.	Zhang W, Liu H, Al-Shabrawey M, et al. Inflammation and diabetic retinal microvascular complications [J]. J Cardiovasc Dis Res, 2011, 2(2): 96-103. DOI: 10.4103/0975-3583.83035.
17.	Costagliola C, Romano V, De Tollis M, et al. TNF-alpha levels in tears: a novel biomarker to assess the degree of diabetic retinopathy [J/OL]. Mediators Inflamm, 2013, 2013: 629529[2013-10-23]. . DOI: 10.1155/2013/629529.
18.	Kuo JZ, Guo X, Klein R, et al. Systemic soluble tumor necrosis factor receptors 1 and 2 are associated with severity of diabetic retinopathy in Hispanics [J]. Ophthalmology, 2012, 119(5): 1041-1046. DOI: 10.1016/j.ophtha.2011.10.040.
19.	Nigro E, Scudiero O, Sarnataro D, et al. Adiponectin affects lung epithelial A549 cell viability counteracting TNFalpha and IL-1ss toxicity through AdipoR1 [J]. Int J Biochem Cell Biol, 2013, 45(6): 1145-1153. DOI: 10.1016/j.biocel.2013.03.003.
20.	Villarreal-Molina MT, Antuna-Puente B. Adiponectin: anti-inflammatory and cardioprotective effects [J]. Biochimie, 2012, 94(10): 2143-21499. DOI: 10.1016/j.biochi.2012.06.030.
21.	Higuchi A, Ohashi K, Kihara S, et al. Adiponectin suppresses pathological microvessel formation in retina through modulation of tumor necrosis factor-alpha expression [J]. Circ Res, 2009, 104(9): 1058-1065. DOI: 10.1161/CIRCRESAHA.109.194506.
22.	Higuchi A, Ohashi K, Shibata R, et al. Thiazolidinediones reduce pathological neovascularization in ischemic retina via an adiponectin-dependent mechanism [J]. Arterioscler Thromb Vasc Biol, 2010, 30(1): 46-53. DOI: 10.1161/ATVBAHA.109.198465.
23.	Ouchi N, Kihara S, Arita Y, et al. Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin [J]. Circulation, 1999, 100(25): 2473-2476.
24.	Engeli S, Feldpausch M, Gorzelniak K, et al. Association between adiponectin and mediators of inflammation in obese women [J]. Diabetes, 2003, 52(4): 942-947.
25.	Matsushita K, Yatsuya H, Tamakoshi K, et al. Inverse association between adiponectin and C-reactive protein in substantially healthy Japanese men [J]. Atherosclerosis, 2006, 188(1): 184-189.
26.	Omae T, Nagaoka T, Tanano I, et al. Adiponectin-induced dilation of isolated porcine retinal arterioles via production of nitric oxide from endothelial cells [J]. Invest Ophthalmol Vis Sci, 2013, 54(7): 4586-4594. DOI: 10.1167/iovs.13-11756.
27.	Omae T, Nagaoka T, Yoshida A. Relationship between retinal blood flow and serum adiponectin concentrations in patients with type 2 diabetes mellitus [J]. Invest Ophthalmol Vis Sci, 2015, 56(6): 4143-4149. DOI: 10.1167/iovs.15-16447.
28.	Nagaoka T, Sato E, Takahashi A, et al. Impaired retinal circulation in patients with type 2 diabetes mellitus: retinal laser Doppler velocimetry study [J]. Invest Ophthalmol Vis Sci, 2010, 51(12): 6729-6734. DOI: 10.1167/iovs.10-5364.
29.	Bora PS, Kaliappan S, Lyzogubov VV, et al. Expression of adiponectin in choroidal tissue and inhibition of laser induced choroidal neovascularization by adiponectin [J]. FEBS Lett, 2007, 581(10): 1977-1982. DOI: 10.1016/j.febslet.2007.04.024.
30.	Mao D, Peng H, Li Q, et al. Aqueous humor and plasma adiponectin levels in proliferative diabetic retinopathy patients [J]. Curr Eye Res, 2012, 37(9): 803-808. DOI: 10.3109/02713683.2012.676700.
31.	Schwarz PE, Towers GW, Fischer S, et al. Hypoadiponectinemia is associated with progression toward type 2 diabetes and genetic variation in the ADIPOQ gene promoter [J]. Diabetes Care, 2006, 29(7): 1645-1650.
32.	Ye E, Yang H, Chen L,et al. Adiponectin and peroxisome proliferator-activated receptor-γ gene polymorphisms and gene-gene interactions with type 2 diabetes[J]. Life Sci, 2014, 98(1): 55-59. DOI: 10.1016/j.lfs.2013.12.232.
33.	Al-Azzam SI, Khabour OF, Alzoubi KH, et al. The role of adiponectin gene variants in glycemic control in patients with type 2 diabetes [J]. Endocr Res, 2014, 39(1): 13-17. DOI: 10.3109/07435800.2013.794427.
34.	Lacquemant C, Froguel P, Lobbens S, et al. The adiponectin gene SNP+45 is associated with coronary artery disease in type 2 (non-insulin-dependent) diabetes mellitus [J]. Diabet Med, 2004, 21(7): 776-781. DOI: 10.1111/j.1464-5491.2004.01224.x.
35.	Kim SH, Kang ES, Hur KY, et al. Adiponectin gene polymorphism 45T>G is associated with carotid artery plaques in patients with type 2 diabetes mellitus [J]. Metabolism, 2008, 57(2): 274-279. DOI: 10.1016/j.metabol.2007.09.012.
36.	El-Shal AS, Zidan HE, Rashad NM. Adiponectin gene polymorphisms in Egyptian type 2 diabetes mellitus patients with and without diabetic nephropathy [J]. Mol Biol Rep, 2014, 41(4): 2287-2298. DOI: 10.1007/s11033-014-3082-0.
37.	Chung HF, Long KZ, Hsu CC, et al. Adiponectin gene (ADIPOQ) polymorphisms correlate with the progression of nephropathy in Taiwanese male patients with type 2 diabetes [J]. Diabetes Res Clin Pract, 2014, 105(2): 261-270. DOI: 10.1016/j.diabres.2014.04.015.
38.	Ji ZY, Li HF, Lei Y, et al. Association of adiponectin gene polymorphisms with an elevated risk of diabetic peripheral neuropathy in type 2 diabetes patients [J]. J Diabetes Complications, 2015, 29(7): 887-892. DOI: 10.1016/j.jdiacomp.2015.06.008.
39.	Rudofsky G Jr, Schlimme M, Schlotterer A, et al. No association of the 94T/G polymorphism in the adiponectin gene with diabetic complications[J]. Diabetes Obes Metab, 2005, 7(4): 455-459.
40.	Yoshioka K, Yoshida T, Takakura Y, et al. Adiponectin gene polymorphism (G276T) and diabetic retinopathy in Japanese patients with type 2 diabetes [J]. Diabet Med, 2004, 21(10): 1158-1159. DOI: 10.1111/j.1464-5491.2004.01308.x.
41.	Choe EY, Wang HJ, Kwon O, et al. Variants of the adiponectin gene and diabetic microvascular complications in patients with type 2 diabetes [J]. Metabolism, 2013, 62(5): 677-685. DOI: 10.1016/j.metabol.2012.11.005.
42.	Li Y, Wu QH, Jiao ML, et al. Gene-environment interaction between adiponectin gene polymorphisms and environmental factors on the risk of diabetic retinopathy [J]. J Diabetes Investig, 2015, 6(1): 56-66. DOI: 10.1111/jdi.12249.

1. Kern PA, Di Gregorio GB,Lu T, et al. Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression[J]. Diabetes, 2003, 52(7): 1779-1785.
2. Lee B, Shao J.Adiponectin and energy homeostasis [J]. Rev Endocr Metab Disord, 2014, 15(2): 149-156. DOI: 10.1007/s11154-013-9283-3.
3. Ohashi K, Ouchi N, Matsuzawa Y. Anti-inflammatory and anti-atherogenic properties of adiponectin [J]. Biochimie, 2012, 94(10): 2137-2142. DOI: 10.1016/j.biochi.2012.06.008.
4. Krenning G, Moonen JR, Harmsen MC. Pleiotropism of adiponectin: inflammation, neovascularization, and fibrosis [J]. Circ Res, 2009, 104(9): 1029-1031. DOI: 10.1161/CIRCRESAHA.109.198044.
5. Kobayashi H, Ouchi N, Kihara S, et al. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin [J]. Circ Res, 2004, 94(4): 27-31. DOI: 10.1161/01.RES.0000119921.86460.37.
6. Yilmaz MI, Sonmez A, Acikel C, et al. Adiponectin may play a part in the pathogenesis of diabetic retinopathy[J]. Eur J Endocrinol, 2004, 151(1): 135-140.
7. Kato K, Osawa H, Ochi M, et al. Serum total and high molecular weight adiponectin levels are correlated with the severity of diabetic retinopathy and nephropathy [J]. Clin Endocrinol (Oxf), 2008, 68(3): 442-449. DOI: 10.1111/j.1365-2265.2007.03063.x.
8. Kuo JZ, Guo X, Klein R, et al. Adiponectin, insulin sensitivity and diabetic retinopathy in latinos with type 2 diabetes [J]. J Clin Endocrinol Metab, 2015, 100(9): 3348-3355. DOI: 10.1210/jc.2015-1221.
9. Pradeepa R, Surendar J, Indulekha K, et al. Association of serum adiponectin with diabetic microvascular complications among south Indian type 2 diabetic subjects - (CURES-133)[J]. Clin Biochem, 2015, 48(1-2): 33-38. DOI: 10.1016/j.clinbiochem.2014.10.009.
10. Matsuda M, Kawasaki F, Yamada K, et al. Impact of adiposity and plasma adipocytokines on diabetic angiopathies in Japanese type 2 diabetic subjects[J]. Diabet Med, 2004, 21(8): 881-888. DOI: 10.1111/j.1464-5491.2004.01261.x.
11. Vionnet N, Hani EH, Dupont S,et al. Genomewide search for type 2 diabetes-susceptibility genes in French whites: evidence for a novel susceptibility locus for early-onset diabetes on chromosome 3q27-qter and independent replication of a type 2-diabetes locus on chromosome 1q21-q24[J]. Am J Hum Genet, 2000, 67(6): 1470-1480.
12. Calton EK, Miller VS, Soares MJ.Factors determining the risk of the metabolic syndrome: is there a central role for adiponectin?[J]. Eur J Clin Nutr, 2013, 67(5): 485-491. DOI: 10.1038/ejcn.2013.1.
13. Kadowaki T, Yamauchi T.Adiponectin and adiponectin receptors[J]. Endocr Rev, 2005, 26(3): 439-451. DOI: 10.1210/er.2005-0005.
14. Lin T, Qiu Y, Liu Y,et al. Expression of adiponectin and its receptors in type 1 diabetes mellitus in human and mouse retinas[J]. Mol Vis, 2013, 19: 1769-1778.
15. Hsu YJ, Wang LC, Yang WS, et al. Effects of fenofibrate on adiponectin expression in retinas of streptozotocin-induced diabetic rats[J/OL].J Diabetes Res, 2014, 2014: 540326 [2014-12-01]. . DOI: 10.1155/2014/540326.
16. Zhang W, Liu H, Al-Shabrawey M, et al. Inflammation and diabetic retinal microvascular complications [J]. J Cardiovasc Dis Res, 2011, 2(2): 96-103. DOI: 10.4103/0975-3583.83035.
17. Costagliola C, Romano V, De Tollis M, et al. TNF-alpha levels in tears: a novel biomarker to assess the degree of diabetic retinopathy [J/OL]. Mediators Inflamm, 2013, 2013: 629529[2013-10-23]. . DOI: 10.1155/2013/629529.
18. Kuo JZ, Guo X, Klein R, et al. Systemic soluble tumor necrosis factor receptors 1 and 2 are associated with severity of diabetic retinopathy in Hispanics [J]. Ophthalmology, 2012, 119(5): 1041-1046. DOI: 10.1016/j.ophtha.2011.10.040.
19. Nigro E, Scudiero O, Sarnataro D, et al. Adiponectin affects lung epithelial A549 cell viability counteracting TNFalpha and IL-1ss toxicity through AdipoR1 [J]. Int J Biochem Cell Biol, 2013, 45(6): 1145-1153. DOI: 10.1016/j.biocel.2013.03.003.
20. Villarreal-Molina MT, Antuna-Puente B. Adiponectin: anti-inflammatory and cardioprotective effects [J]. Biochimie, 2012, 94(10): 2143-21499. DOI: 10.1016/j.biochi.2012.06.030.
21. Higuchi A, Ohashi K, Kihara S, et al. Adiponectin suppresses pathological microvessel formation in retina through modulation of tumor necrosis factor-alpha expression [J]. Circ Res, 2009, 104(9): 1058-1065. DOI: 10.1161/CIRCRESAHA.109.194506.
22. Higuchi A, Ohashi K, Shibata R, et al. Thiazolidinediones reduce pathological neovascularization in ischemic retina via an adiponectin-dependent mechanism [J]. Arterioscler Thromb Vasc Biol, 2010, 30(1): 46-53. DOI: 10.1161/ATVBAHA.109.198465.
23. Ouchi N, Kihara S, Arita Y, et al. Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin [J]. Circulation, 1999, 100(25): 2473-2476.
24. Engeli S, Feldpausch M, Gorzelniak K, et al. Association between adiponectin and mediators of inflammation in obese women [J]. Diabetes, 2003, 52(4): 942-947.
25. Matsushita K, Yatsuya H, Tamakoshi K, et al. Inverse association between adiponectin and C-reactive protein in substantially healthy Japanese men [J]. Atherosclerosis, 2006, 188(1): 184-189.
26. Omae T, Nagaoka T, Tanano I, et al. Adiponectin-induced dilation of isolated porcine retinal arterioles via production of nitric oxide from endothelial cells [J]. Invest Ophthalmol Vis Sci, 2013, 54(7): 4586-4594. DOI: 10.1167/iovs.13-11756.
27. Omae T, Nagaoka T, Yoshida A. Relationship between retinal blood flow and serum adiponectin concentrations in patients with type 2 diabetes mellitus [J]. Invest Ophthalmol Vis Sci, 2015, 56(6): 4143-4149. DOI: 10.1167/iovs.15-16447.
28. Nagaoka T, Sato E, Takahashi A, et al. Impaired retinal circulation in patients with type 2 diabetes mellitus: retinal laser Doppler velocimetry study [J]. Invest Ophthalmol Vis Sci, 2010, 51(12): 6729-6734. DOI: 10.1167/iovs.10-5364.
29. Bora PS, Kaliappan S, Lyzogubov VV, et al. Expression of adiponectin in choroidal tissue and inhibition of laser induced choroidal neovascularization by adiponectin [J]. FEBS Lett, 2007, 581(10): 1977-1982. DOI: 10.1016/j.febslet.2007.04.024.
30. Mao D, Peng H, Li Q, et al. Aqueous humor and plasma adiponectin levels in proliferative diabetic retinopathy patients [J]. Curr Eye Res, 2012, 37(9): 803-808. DOI: 10.3109/02713683.2012.676700.
31. Schwarz PE, Towers GW, Fischer S, et al. Hypoadiponectinemia is associated with progression toward type 2 diabetes and genetic variation in the ADIPOQ gene promoter [J]. Diabetes Care, 2006, 29(7): 1645-1650.
32. Ye E, Yang H, Chen L,et al. Adiponectin and peroxisome proliferator-activated receptor-γ gene polymorphisms and gene-gene interactions with type 2 diabetes[J]. Life Sci, 2014, 98(1): 55-59. DOI: 10.1016/j.lfs.2013.12.232.
33. Al-Azzam SI, Khabour OF, Alzoubi KH, et al. The role of adiponectin gene variants in glycemic control in patients with type 2 diabetes [J]. Endocr Res, 2014, 39(1): 13-17. DOI: 10.3109/07435800.2013.794427.
34. Lacquemant C, Froguel P, Lobbens S, et al. The adiponectin gene SNP+45 is associated with coronary artery disease in type 2 (non-insulin-dependent) diabetes mellitus [J]. Diabet Med, 2004, 21(7): 776-781. DOI: 10.1111/j.1464-5491.2004.01224.x.
35. Kim SH, Kang ES, Hur KY, et al. Adiponectin gene polymorphism 45T>G is associated with carotid artery plaques in patients with type 2 diabetes mellitus [J]. Metabolism, 2008, 57(2): 274-279. DOI: 10.1016/j.metabol.2007.09.012.
36. El-Shal AS, Zidan HE, Rashad NM. Adiponectin gene polymorphisms in Egyptian type 2 diabetes mellitus patients with and without diabetic nephropathy [J]. Mol Biol Rep, 2014, 41(4): 2287-2298. DOI: 10.1007/s11033-014-3082-0.
37. Chung HF, Long KZ, Hsu CC, et al. Adiponectin gene (ADIPOQ) polymorphisms correlate with the progression of nephropathy in Taiwanese male patients with type 2 diabetes [J]. Diabetes Res Clin Pract, 2014, 105(2): 261-270. DOI: 10.1016/j.diabres.2014.04.015.
38. Ji ZY, Li HF, Lei Y, et al. Association of adiponectin gene polymorphisms with an elevated risk of diabetic peripheral neuropathy in type 2 diabetes patients [J]. J Diabetes Complications, 2015, 29(7): 887-892. DOI: 10.1016/j.jdiacomp.2015.06.008.
39. Rudofsky G Jr, Schlimme M, Schlotterer A, et al. No association of the 94T/G polymorphism in the adiponectin gene with diabetic complications[J]. Diabetes Obes Metab, 2005, 7(4): 455-459.
40. Yoshioka K, Yoshida T, Takakura Y, et al. Adiponectin gene polymorphism (G276T) and diabetic retinopathy in Japanese patients with type 2 diabetes [J]. Diabet Med, 2004, 21(10): 1158-1159. DOI: 10.1111/j.1464-5491.2004.01308.x.
41. Choe EY, Wang HJ, Kwon O, et al. Variants of the adiponectin gene and diabetic microvascular complications in patients with type 2 diabetes [J]. Metabolism, 2013, 62(5): 677-685. DOI: 10.1016/j.metabol.2012.11.005.
42. Li Y, Wu QH, Jiao ML, et al. Gene-environment interaction between adiponectin gene polymorphisms and environmental factors on the risk of diabetic retinopathy [J]. J Diabetes Investig, 2015, 6(1): 56-66. DOI: 10.1111/jdi.12249.

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