Research progress on the biological clock genes and diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhou Qi ^1,2 , Lu Fang ³ ,  Ye Hejiang ²

1. Eye School, Chengdu University of Traditional Chinese Medicine, Chengdu 610072, China;
2. Department of Ophthalmology, Affiliated Hospital of Chengdu University of Traditional Chinese Medicine, Chengdu 610075, China;
3. Department of Ophthalmology, West China Hospital of Sichuan University, Chengdu 610041, China;

Corresponding author：

Ye Hejiang, Email: yehej@163.com

Keywords：

Diabetic retinopathy; Diabetes mellitus; Biological clock genes; Circadian rhythm

DOI：

10.3760/cma.j.cn511434-20210710-00371

Video：

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Diabetic retinopathy (DR) is one of the most common and serious complication of diabetes mellitus, which is the main cause of vision loss in adults. Biological clock genes produce circadian rhythms and control its operation, while the disorder of the expression causes the occurrence and development of a series of diseases. It has been demonstrated that biological clock genes might take effects in the development and progression of DR. On the one hand, circadian rhythm disorder-related behavior disrupts the circadian oscillation of clock genes, and the change in its expression level is prone to unbalanced regulation of glucose metabolism, ultimately increasing the risk of type 2 diabetes mellitus and DR pathogenesis. On the other hand, DR patients exhibit symptoms of circadian rhythm disorders, and it has been suggested that the clock genes may control the development and progression of DR by affecting a variety of retinal pathophysiological processes. Therefore, maintaining normal circadian rhythm can be used as a disease prevention strategy, and studying the molecular mechanism of clock genes in DR can provide new ideas for more comprehensive elaboration of the pathogenesis of DR and search for new therapeutic targets.

Citation： Zhou Qi, Lu Fang, Ye Hejiang. Research progress on the biological clock genes and diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2023, 39(1): 78-82. doi: 10.3760/cma.j.cn511434-20210710-00371 Copy

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3.	Ostrin LA, Jnawali A, Carkeet A, et al. Twenty-four hour ocular and systemic diurnal rhythms in children[J]. Ophthalmic Physiol Opt, 2019, 39(5): 358-369. DOI: 10.1111/opo.12633.
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5.	Suwazono Y, Dochi M, Oishi M, et al. Shiftwork and impaired glucose metabolism: a 14-year cohort study on 7104 male workers[J]. Chronobiol Int, 2009, 26(5): 926-941. DOI: 10.1080/07420520903044422.
6.	Vetter C, Scheer F. A healthy lifestyle-reducing T2DM risk in shift workers?[J]. Nat Rev Endocrinol, 2019, 15(4): 194-196. DOI: 10.1038/s41574-019-0164-z.
7.	Qian JY, Block GD, Colwell CS, et al. Consequences of exposure to light at night on the pancreatic islet circadian clock and function in rats[J]. Diabetes, 2013, 62(10): 3469-3478. DOI: 10.2337/db12-1543.
8.	Wu T, ZhuGe F, Sun L, et al. Enhanced effect of daytime restricted feeding on the circadian rhythm of streptozotocin-induced type 2 diabetic rats[J/OL]. Am J Physiol-Endoc M, 2012, 302(9): E1027-1035[2021-05-15]. https://pubmed.ncbi.nlm.nih.gov/22318948/. DOI: 10.1152/ajpendo.00651.2011.
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1. Bhatwadekar AD, Rameswara V. Circadian rhythms in diabetic retinopathy: an overview of pathogenesis and investigational drugs[J]. Expert Opin Investig Drugs, 2020, 29(12): 1431-1442. DOI: 10.1080/13543784.2020.1842872.
2. 陈筵明, 龚维坤, 孙英芬, 等. 昼夜节律紊乱与2型糖尿病关系的研究进展[J]. 中国细胞生物学学报, 2020, 42(9): 1684-1693. DOI: 10.11844/cjcb.2020.09.0023.Chen YM, Gong WK, Sun YF, et al. Progress in the study of the relationship between circadian rhythm disruption and type 2 diabetes mellitus[J]. Chinese Journal of Cell Biology, 2020, 42(9): 1684-1693. DOI: 10.11844/cjcb.2020.09.0023.
3. Ostrin LA, Jnawali A, Carkeet A, et al. Twenty-four hour ocular and systemic diurnal rhythms in children[J]. Ophthalmic Physiol Opt, 2019, 39(5): 358-369. DOI: 10.1111/opo.12633.
4. Felder-Schmittbuhl MP, Calligaro H, Dkhissi-Benyahya O. The retinal clock in mammals: role in health and disease[J]. ChronoPhysiology and Therapy, 2017, 7: 33-45. DOI: 10.2147/CPT.S115251.
5. Suwazono Y, Dochi M, Oishi M, et al. Shiftwork and impaired glucose metabolism: a 14-year cohort study on 7104 male workers[J]. Chronobiol Int, 2009, 26(5): 926-941. DOI: 10.1080/07420520903044422.
6. Vetter C, Scheer F. A healthy lifestyle-reducing T2DM risk in shift workers?[J]. Nat Rev Endocrinol, 2019, 15(4): 194-196. DOI: 10.1038/s41574-019-0164-z.
7. Qian JY, Block GD, Colwell CS, et al. Consequences of exposure to light at night on the pancreatic islet circadian clock and function in rats[J]. Diabetes, 2013, 62(10): 3469-3478. DOI: 10.2337/db12-1543.
8. Wu T, ZhuGe F, Sun L, et al. Enhanced effect of daytime restricted feeding on the circadian rhythm of streptozotocin-induced type 2 diabetic rats[J/OL]. Am J Physiol-Endoc M, 2012, 302(9): E1027-1035[2021-05-15]. https://pubmed.ncbi.nlm.nih.gov/22318948/. DOI: 10.1152/ajpendo.00651.2011.
9. Perelis M, Marcheva B, Ramsey KM, et al. Pancreatic beta cell enhancers regulate rhythmic transcription of genes controlling insulin secretion[J/OL]. Science, 2015, 350(6261): aac4250[2015-11-06]. https://pubmed.ncbi.nlm.nih.gov/26542580/. DOI: 10.1126/science.aac4250.
10. Ding GL, Li X, Hou XG, et al. REV-ERB in GABAergic neurons controls diurnal hepatic insulin sensitivity[J]. Nature, 2021, 592(7856): 763-767. DOI: 10.1038/s41586-021-03358-w.
11. Pulimeno P, Mannic T, Sage D, et al. Autonomous and self-sustained circadian oscillators displayed in human islet cells[J]. Diabetologia, 2013, 56(3): 497-507. DOI: 10.1007/s00125-012-2779-7.
12. Corella D, Asensio EM, Coltell O, et al. CLOCK gene variation is associated with incidence of type-2 diabetes and cardiovascular diseases in type-2 diabetic subjects: dietary modulation in the PREDIMED randomized trial[J]. Cardiovasc Diabetol, 2016, 15: 4. DOI: 10.1186/s12933-015-0327-8.
13. Marcheva B, Ramsey KM, Buhr ED, et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes[J]. Nature, 2010, 466(7306): 627-631. DOI: 10.1038/nature09253.
14. Vieira E, Merino B, Quesada I. Role of the clock gene Rev-erbalpha in metabolism and in the endocrine pancreas[J]. Diabetes Obes Metab, 2015, 17: 106-114. DOI: 10.1111/dom.12522.
15. Barclay JL, Shostak A, Leliavski A, et al. High-fat diet-induced hyperinsulinemia and tissue-specific insulin resistance in Cry-deficient mice[J/OL]. Am J Physiol Endocrinol Metab, 2013, 304(10): E1053-1063[2013-05-15]. https://pubmed.ncbi.nlm.nih.gov/23531614/. DOI: 10.1152/ajpendo.00512.2012.
16. 张翕宇, 晁俊, 王鹤亭, 等. 参芪复方对2型糖尿病GK大鼠生理节律的影响[J]. 实用医学杂志, 2020, 36(7): 874-879. DOI: 10.3969/j.issn.1006-5725.2020.07.009.Zhang XY, Chao J, Wang HT, et al. Effect of Shenqi compound on physiological rhythm in type 2 diabetic GK rats[J]. The Journal of Practical Medicine, 2020, 36(7): 874-879. DOI: 10.3969/j.issn.1006-5725.2020.07.009.
17. Ribas-Latre A, Fekry B, Kwok C, et al. Rosiglitazone reverses high fat diet-induced changes in BMAL1 function in muscle, fat, and liver tissue in mice[J]. Int J Obes (Lond), 2019, 43(3): 567-580. DOI: 10.1038/s41366-018-0090-5.
18. Wang K, Sun Y, Lin P, et al. Liraglutide activates AMPK signaling and partially restores normal circadian rhythm and insulin secretion in pancreatic islets in diabetic mice[J]. Biol Pharm Bull, 2015, 38(8): 1142-1149. DOI: 10.1248/bpb.b15-00024.
19. McMahon DG, Iuvone PM, Tosini G. Circadian organization of the mammalian retina: from gene regulation to physiology and diseases[J]. Prog Retin Eye Res, 2014, 39: 58-76. DOI: 10.1016/j.preteyeres.2013.12.001.
20. Storch KF, Paz C, Signorovitch J, et al. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information[J]. Cell, 2007, 130(4): 730-741. DOI: 10.1016/j.cell.2007.06.045.
21. Dutta S, Ghosh S, Ghosh S. Association of sleep disturbance with diabetic retinopathy[J]. Eur J Ophthalmol, 2022, 32(1): 468-474. DOI: 10.1177/1120672120974296.
22. Kim YS, Davis SCAT, Stok WJ, et al. Impaired nocturnal blood pressure dipping in patients with type 2 diabetes mellitus[J]. Hypertens Res, 2019, 42(1): 59-66. DOI: 10.1038/s41440-018-0130-5.
23. Knudsen ST, Poulsen PL, Hansen KW, et al. Pulse pressure and diurnal blood pressure variation: association with micro- and macrovascular complications in type 2 diabetes[J]. Am J Hypertens, 2002, 15(3): 244-250. DOI: 10.1016/s0895-7061(01)02281-6.
24. Di R, Luo Q, Mathew D, et al. Diabetes alters diurnal rhythm of electroretinogram in db/db mice[J]. Yale J Biol Med, 2019, 92(2): 155-167.
25. Polito A, Del Borrello M, Polini G, et al. Diurnal variation in clinically significant diabetic macular edema measured by the stratus OCT[J]. Retina, 2006, 26(1): 14-20. DOI: 10.1097/00006982-200601000-00003.
26. Busik JV, Tikhonenko M, Bhatwadekar A, et al. Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock[J]. J Exp Med, 2009, 206(13): 2897-2906. DOI: 10.1084/jem.20090889.
27. Wang Q, Tikhonenko M, Bozack SN, et al. Changes in the daily rhythm of lipid metabolism in the diabetic retina[J/OL]. PLoS One, 2014, 9(4): e95028[2014-04-15]. https://pubmed.ncbi.nlm.nih.gov/24736612/. DOI: 10.1371/journal.pone.0095028.
28. Lahouaoui H, Coutanson C, Cooper HM, et al. Diabetic retinopathy alters light-induced clock gene expression and dopamine levels in the mouse retina[J]. Mol Vis, 2016, 22: 959-969.
29. Lyons TJ, Jenkins AJ, Zheng D, et al. Diabetic retinopathy and serum lipoprotein subclasses in the DCCT/EDIC cohort[J]. Invest Ophthalmol Vis Sci, 2004, 45(3): 910-918. DOI: 10.1167/iovs.02-0648.
30. Chang YC, Wu WC. Dyslipidemia and diabetic retinopathy[J]. Rev Diabet Stud, 2013, 10(2-3): 121-132. DOI: 10.1900/RDS.2013.10.121.
31. Fu Z, Chen CT, Cagnone G, et al. Dyslipidemia in retinal metabolic disorders[J/OL]. EMBO Mol Med, 2019, 11(10): e10473[2019-09-05].https://pubmed.ncbi.nlm.nih.gov/31486227/. DOI: 10.15252/emmm.201910473.
32. Matsumoto E, Ishihara A, Tamai S, et al. Time of day and nutrients in feeding govern daily expression rhythms of the gene for sterol regulatory element-binding protein (SREBP)-1 in the mouse liver[J]. J Biol Chem, 2010, 285(43): 33028-33036. DOI: 10.1074/jbc.M109.089391.
33. Canaple L, Rambaud J, Dkhissi-Benyahya O, et al. Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferator-activated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock[J]. Mol Endocrinol, 2006, 20(8): 1715-1727. DOI: 10.1210/me.2006-0052.
34. Wang N, Yang G, Jia Z, et al. Vascular PPARγ controls circadian variation in blood pressure and heart rate through Bmal1[J]. Cell Metabolism, 2008, 8(6): 482-491. DOI: 10.1016/j.cmet.2008.10.009.
35. Berdeaux O, Acar N. Very-long-chain polyunsaturated fatty acids in the retina: analysis and clinical relevance in physiological and pathological conditions[J]. Oléagineux, Corps gras, Lipides, 2011, 18(5): 284-290. DOI: 10.1051/ocl.2011.0406.
36. Tikhonenko M, Lydic TA, Wang Y, et al. Remodeling of retinal Fatty acids in an animal model of diabetes: a decrease in long-chain polyunsaturated fatty acids is associated with a decrease in fatty acid elongases Elovl2 and Elovl4[J]. Diabetes, 2010, 59(1): 219-227. DOI: 10.2337/db09-0728.
37. 黎晓新, 白玉婧. 重视Müller细胞在糖尿病视网膜病变中作用的基础研究[J]. 中华眼科杂志, 2015, 51(5): 321-322. DOI: 10.3760/cma.j.issn.0412-4081.2015.05.001.Li XX, Bai YJ. To attach importance of basic research in Müller cell of diabetic retinopathy[J]. Chin J Ophthalmol, 2015, 51(5): 321-322. DOI: 10.3760/cma.j.issn.0412-4081.2015.05.001.
38. Xu L, Ruan G, Dai H, et al. Mammalian retinal Müller cells have circadian clock function[J]. Molecular Vision, 2016, 22: 275-283.
39. Xu LL, Penn J, McMahon D. Circadian clock gene regulation of retinal neovascularization[C]. ARVO Annual Meeing, Seattle, The United States, 2013.
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Advances in single-cell RNA sequencing in the retina

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Research progress on the biological clock genes and diabetic retinopathy

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