Research progress of miRNA in age-related macular degeneration_Chinese Journal of Ocular Fundus Diseases

Authors：

Gao Jingfan ,  Zhang Lu

Ophthalmology Hospital of The First Affiliated Hospital of Harbin Medical University, Harbin 150001, China;

Corresponding author：

Zhang Lu, Email: 13796089809@163.com

Keywords：

Macular degeneration; MicroRNAs; Oxidative stress; Neovascularization, pathologic; Inflammation; Review

DOI：

10.3760/cma.j.cn511434-20200312-00109

Video：

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Age-related macular degeneration (AMD) is a multifactorial disease affected by environmental factors and genetic variation, which is a major cause of irreversible vision loss in the elderly. miRNA is a kind of endogenous non-coding RNA, which plays an important role in the pathogenesis of AMD, such as oxidative stress, pathological neovascularization and inflammation, by inhibiting or silencing the expression of transcription genes. miRNA has unique advantages in terms of ease synthesis, targeting and additive effect, a large number of experiments have proved the therapeutic potential of miRNA in AMD, which is expected to become a new method for the treatment of AMD in the future. Since the pathogenesis of AMD has not been fully elucidated, it is still necessary to continue to study the pathogenesis of AMD, the biological effects and mechanisms of various miRNA in the occurrence and development of AMD, and observe its therapeutic effects in AMD, so as to provide more effective options for the precise prevention and treatment of AMD.

Citation： Gao Jingfan, Zhang Lu. Research progress of miRNA in age-related macular degeneration. Chinese Journal of Ocular Fundus Diseases, 2021, 37(6): 488-491. doi: 10.3760/cma.j.cn511434-20200312-00109 Copy

1.	Mitchell P, Liew G, Gopinath B, et al. Age-related macular degeneration[J]. Lancet, 2018, 392(10153): 1147-1159. DOI: 10.1016/S0140-6736(18)31550-2.
2.	Askou AL, Alsing S, Holmgaard A, et al. Dissecting microRNA dysregulation in age-related macular degeneration: new targets for eye gene therapy[J]. Acta Ophthalmol, 2018, 96(1): 9-23. DOI: 10.1111/aos.13407.
3.	潘俊如, 余其林, 张述, 等. 老年性黄斑变性病因研究新进展[J]. 国际眼科杂志, 2013, 13(5): 905-908. DOI: 10.3980/j.issn.1672-5123.2013.05.18.Pan JR, Yu QL, Zhang S, et al. Advance in etiology of age-related macular degenerationy[J]. Int Eye Sci, 2013, 13(5): 905-908. DOI: 10.3980/j.issn.1672-5123.2013.05.18.
4.	Murad N, Kokkinaki M, Gunawardena N, et al. MiR-184 regulates ezrin, LAMP‐1 expression, affects phagocytosis in human retinal pigment epithelium and is downregulated in age-related macular degeneration[J]. FEBS J, 2014, 281(23): 5251-5264. DOI: 10.1111/febs.13066.
5.	秦兵. MicroRNA-184调控视网膜色素上皮细胞分化机制的研究[D]. 南京: 南京医科大学, 2018.Qin B. Study on the mechanism of microRNA-184 regulating the differentiation of retinal pigment epithelial cells[D]. Nanjing: Nanjing Medical University, 2018.
6.	Lin H, Qian J, Castillo AC, et al. Effect of miR-23 on oxidant-induced injury in human retinal pigment epithelial cells[J]. Invest Ophthalmol Vis Sci, 2011, 52(9): 6308-6314. DOI: 10.1167/iovs.10-6632.
7.	Tasharrofi N, Kouhkan F, Soleimani M, et al. Survival improvement in human retinal pigment epithelial cells via Fas receptor targeting by miR-374a[J]. J Cell Biochem, 2017, 118(12): 4854-4861. DOI: 10.1002/jcb.26160.
8.	Li DD, Zhong BW, Zhang HX, et al. Inhibition of the oxidative stress-induced miR-23a protects the human retinal pigment epithelium (RPE) cells from apoptosis through the upregulation of glutaminase and glutamine uptake[J]. Mol Biol Rep, 2016, 43(10): 1079-1087. DOI: 10.1007/s11033-016-4041-8.
9.	Ayaz L, Dinc E. Evaluation of microRNA responses in ARPE-19 cells against the oxidative stress[J]. Cutan Ocul Toxicol, 2018, 37(2): 121-126. DOI: 10.1080/15569527.2017.1355314.
10.	Haque R, Chun E, Howell JC, et al. MicroRNA-30b-mediated regulation of catalase expression in human ARPE-19 cells[J/OL]. PLoS One, 2012, 7(8): e42542[2012-08-06]. https://pubmed.ncbi.nlm.nih.gov/22880027/. DOI: 10.1371/journal.pone.0042542.
11.	Tian B, Maidana DE, Dib B, et al. MiR-17-3p exacerbates oxidative damage in human retinal pigment epithelial cells[J/OL]. PLoS One, 2016, 11(8): e0160887[2016-08-09]. https://pubmed.ncbi.nlm.nih.gov/27505139/. DOI: 10.1371/journal.pone.0160887.
12.	Jadeja RN, Jones MA, Abdelrahman AA, et al. Inhibiting microRNA-144 potentiates Nrf2-dependent antioxidant signaling in RPE and protects against oxidative stress-induced outer retinal degeneration[J/OL]. Redox Biol, 2020, 1(28): 101336[2019-09-29]. https://pubmed.ncbi.nlm.nih.gov/31590045/. DOI: 10.1016/j.redox.2019.101336.
13.	Sun W, Zhao L, Song X, et al. MicroRNA-210 modulates the cellular energy metabolism shift during H₂O₂-induced oxidative stress by repressing ISCU in H9c2 cardiomyocytes[J]. Cell Physiol Biochem, 2017, 43(1): 383-394. DOI: 10.1159/000480417.
14.	Talepoor AM, Rostamian DM, Baghi M, et al. Upregulation of miR-200a and miR-204 in MPP+‐treated differentiated PC12 cells as a model of Parkinson’s disease[J/OL]. Mol Genet Genomic Med, 2019, 7(3): e548[2019-02-03]. https://pubmed.ncbi.nlm.nih.gov/30712312/. DOI: 10.1159/000480417.
15.	Zhou Q, Anderson C, Zhang H, et al. Repression of choroidal neovascularization through actin cytoskeleton pathways by microRNA-24[J]. Mol Ther, 2014, 22(2): 378-389. DOI: 10.1038/mt.2013.243.
16.	Lu JM, Zhang ZZ, Ma X, et al. Repression of microRNA-21 inhibits retinal vascular endothelial cell growth and angiogenesis via PTEN dependent-PI3K/Akt/VEGF signaling pathway in diabetic retinopathy[J/OL]. Exp Eye Res, 2020, 1(190): 107886[2019-11-21]. https://pubmed.ncbi.nlm.nih.gov/31759996/. DOI: 10.1016/j.exer.2019.107886.
17.	Lin JB, Moolani HV, Sene A, et al. Macrophage microRNA-150 promotes pathological angiogenesis as seen in age-related macular degeneration[J/OL]. JCI insight, 2018, 3(7): e120157[2018-04-05]. https://pubmed.ncbi.nlm.nih.gov/29618664/. DOI: 10.1172/jci.insight.120157.
18.	Wang L, Lee AY, Wigg JP, et al. MiR-126 regulation of angiogenesis in age-related macular degeneration in CNV mouse model[J/OL]. Int J Mol Sci, 2016, 17(6): 895[2016-06-07]. https://pubmed.ncbi.nlm.nih.gov/27338342/. DOI: 10.3390/ijms17060895.
19.	Westenskow PD, Kurihara T, Aguilar E, et al. Ras pathway inhibition prevents neovascularization by repressing endothelial cell sprouting[J]. J Clin Invest, 2013, 123(11): 4900-4908. DOI: 10.1172/JCI70230.
20.	Nunes DN, Dias-Neto E, Cardó-Vila M, et al. Synchronous down-modulation of miR-17 family members is an early causative event in the retinal angiogenic switch[J]. Proc Natl Acad Sci USA, 2015, 112(12): 3770-3775. DOI: 10.1073/pnas.1500008112.
21.	Liu CH, Huang S, BrittonWR, et al. MicroRNAs in vascular eye diseases[J/OL]. Int J Mol Sci, 2020, 21(2): 649[2019-01-19]. https://pubmed.ncbi.nlm.nih.gov/31963809/. DOI: 10.3390/ijms21020649.
22.	Blasiak J, Watala C, Tuuminen R, et al. Expression of VEGFA-regulating miRNAs and mortality in wet AMD[J]. J Cell Mol Med, 2019, 23(12): 8464-8471. DOI: 10.1111/jcmm.14731.
23.	Elbay A, Ercan Ç, Akbaş F, et al. Three new circulating microRNAs may be associated with wet age-related macular degeneration[J]. Scand J Clin Lab Invest, 2019, 79(6): 388-394. DOI: 10.1080/00365513.2019.1637931.
24.	Walz JM, Wecker T, Zhang PP, et al. Impact of angiogenic activation and inhibition on miRNA profiles of human retinal endothelial cells[J]. Exp Eye Res, 2019, 4(181): 98-104. DOI: 10.1016/j.exer.2019.01.006.
25.	Lian C, Lou H, Zhang J, et al. MicroRNA-24 protects retina from degeneration in rats by down-regulating chitinase-3-like protein 1[J/OL]. Exp Eye Res, 2019, 9(188): 107791[2019-09-03]. https://pubmed.ncbi.nlm.nih.gov/31491426/. DOI: 10.1016/j.exer.2019.107791.
26.	Chu-Tan JA, Rutar M, Saxena K, et al. MicroRNA-124 dysregulation is associated with retinal inflammation and photoreceptor death in the degenerating retina[J]. Invest Ophthalmol Vis Sci, 2018, 59(10): 4094-4105. DOI: 10.1167/iovs.18-24623.
27.	Liu J, Ma Z, Ran Z. MiR-21-3p modulates lipopolysaccharide-induced inflammation and apoptosis via targeting TGS 4 in retinal pigment epithelial cells[J]. Clin Exp Pharmacol Physiol, 2019, 46(10): 883-889. DOI: 10.1111/1440-1681.13142.
28.	Cheng Y, Du L, Jiao H, et al. Mmu-miR-27a-5p-dependent upregulation of MCPIP1 inhibits the inflammatory response in LPS-induced RAW264.7 macrophage cells[J/OL]. Biomed Res Int, 2015, 2015: 607692[2015-07-30]. https://pubmed.ncbi.nlm.nih.gov/26295043/. DOI: 10.1155/2015/607692.
29.	SanGiovanni JP, SanGiovanni PM, Sapieha P, et al. miRNAs, single nucleotide polymorphisms (SNPs) and age-related macular degeneration (AMD)[J]. Clin Chem Lab Med, 2017, 55(5): 763-775. DOI: 10.1515/cclm-2016-0898.
30.	Bhattacharjee S, Zhao Y, Dua P, et al. MicroRNA-34a-mediated down-regulation of the microglial-enriched triggering receptor and phagocytosis-sensor TREM2 in age-related macular degeneration[J/OL]. PLoS One, 2016, 11(3): e0150211[2016-03-07]. https://pubmed.ncbi.nlm.nih.gov/26949937/. DOI: 10.1371/journal.pone.0150211.
31.	Huang P, Sun J, Wang F, et al. MicroRNA expression patterns involved in amyloid beta-induced retinal degeneration[J]. Invest Ophthalmol Vis Sci, 2017, 58(3): 1726-1735. DOI: 10.1167/iovs.16-20043.
32.	To KKW, Fong W, Tong CWS, et al. Advances in the discovery of microRNA-based anticancer therapeutics: latest tools and developments[J]. Expert Opin Drug Discov, 2020, 15(1): 63-83. DOI: 10.1080/17460441.2020.1690449.
33.	Askou AL, Alsing S, Benckendorff JNE, et al. Suppression of choroidal neovascularization by AAV-based dual-acting antiangiogenic gene therapy[J]. Mol Ther Nucleic Acids, 2019, 16: 38-50. DOI: 10.1016/j.omtn.2019.01.012.

1. Mitchell P, Liew G, Gopinath B, et al. Age-related macular degeneration[J]. Lancet, 2018, 392(10153): 1147-1159. DOI: 10.1016/S0140-6736(18)31550-2.
2. Askou AL, Alsing S, Holmgaard A, et al. Dissecting microRNA dysregulation in age-related macular degeneration: new targets for eye gene therapy[J]. Acta Ophthalmol, 2018, 96(1): 9-23. DOI: 10.1111/aos.13407.
3. 潘俊如, 余其林, 张述, 等. 老年性黄斑变性病因研究新进展[J]. 国际眼科杂志, 2013, 13(5): 905-908. DOI: 10.3980/j.issn.1672-5123.2013.05.18.Pan JR, Yu QL, Zhang S, et al. Advance in etiology of age-related macular degenerationy[J]. Int Eye Sci, 2013, 13(5): 905-908. DOI: 10.3980/j.issn.1672-5123.2013.05.18.
4. Murad N, Kokkinaki M, Gunawardena N, et al. MiR-184 regulates ezrin, LAMP‐1 expression, affects phagocytosis in human retinal pigment epithelium and is downregulated in age-related macular degeneration[J]. FEBS J, 2014, 281(23): 5251-5264. DOI: 10.1111/febs.13066.
5. 秦兵. MicroRNA-184调控视网膜色素上皮细胞分化机制的研究[D]. 南京: 南京医科大学, 2018.Qin B. Study on the mechanism of microRNA-184 regulating the differentiation of retinal pigment epithelial cells[D]. Nanjing: Nanjing Medical University, 2018.
6. Lin H, Qian J, Castillo AC, et al. Effect of miR-23 on oxidant-induced injury in human retinal pigment epithelial cells[J]. Invest Ophthalmol Vis Sci, 2011, 52(9): 6308-6314. DOI: 10.1167/iovs.10-6632.
7. Tasharrofi N, Kouhkan F, Soleimani M, et al. Survival improvement in human retinal pigment epithelial cells via Fas receptor targeting by miR-374a[J]. J Cell Biochem, 2017, 118(12): 4854-4861. DOI: 10.1002/jcb.26160.
8. Li DD, Zhong BW, Zhang HX, et al. Inhibition of the oxidative stress-induced miR-23a protects the human retinal pigment epithelium (RPE) cells from apoptosis through the upregulation of glutaminase and glutamine uptake[J]. Mol Biol Rep, 2016, 43(10): 1079-1087. DOI: 10.1007/s11033-016-4041-8.
9. Ayaz L, Dinc E. Evaluation of microRNA responses in ARPE-19 cells against the oxidative stress[J]. Cutan Ocul Toxicol, 2018, 37(2): 121-126. DOI: 10.1080/15569527.2017.1355314.
10. Haque R, Chun E, Howell JC, et al. MicroRNA-30b-mediated regulation of catalase expression in human ARPE-19 cells[J/OL]. PLoS One, 2012, 7(8): e42542[2012-08-06]. https://pubmed.ncbi.nlm.nih.gov/22880027/. DOI: 10.1371/journal.pone.0042542.
11. Tian B, Maidana DE, Dib B, et al. MiR-17-3p exacerbates oxidative damage in human retinal pigment epithelial cells[J/OL]. PLoS One, 2016, 11(8): e0160887[2016-08-09]. https://pubmed.ncbi.nlm.nih.gov/27505139/. DOI: 10.1371/journal.pone.0160887.
12. Jadeja RN, Jones MA, Abdelrahman AA, et al. Inhibiting microRNA-144 potentiates Nrf2-dependent antioxidant signaling in RPE and protects against oxidative stress-induced outer retinal degeneration[J/OL]. Redox Biol, 2020, 1(28): 101336[2019-09-29]. https://pubmed.ncbi.nlm.nih.gov/31590045/. DOI: 10.1016/j.redox.2019.101336.
13. Sun W, Zhao L, Song X, et al. MicroRNA-210 modulates the cellular energy metabolism shift during H₂O₂-induced oxidative stress by repressing ISCU in H9c2 cardiomyocytes[J]. Cell Physiol Biochem, 2017, 43(1): 383-394. DOI: 10.1159/000480417.
14. Talepoor AM, Rostamian DM, Baghi M, et al. Upregulation of miR-200a and miR-204 in MPP+‐treated differentiated PC12 cells as a model of Parkinson’s disease[J/OL]. Mol Genet Genomic Med, 2019, 7(3): e548[2019-02-03]. https://pubmed.ncbi.nlm.nih.gov/30712312/. DOI: 10.1159/000480417.
15. Zhou Q, Anderson C, Zhang H, et al. Repression of choroidal neovascularization through actin cytoskeleton pathways by microRNA-24[J]. Mol Ther, 2014, 22(2): 378-389. DOI: 10.1038/mt.2013.243.
16. Lu JM, Zhang ZZ, Ma X, et al. Repression of microRNA-21 inhibits retinal vascular endothelial cell growth and angiogenesis via PTEN dependent-PI3K/Akt/VEGF signaling pathway in diabetic retinopathy[J/OL]. Exp Eye Res, 2020, 1(190): 107886[2019-11-21]. https://pubmed.ncbi.nlm.nih.gov/31759996/. DOI: 10.1016/j.exer.2019.107886.
17. Lin JB, Moolani HV, Sene A, et al. Macrophage microRNA-150 promotes pathological angiogenesis as seen in age-related macular degeneration[J/OL]. JCI insight, 2018, 3(7): e120157[2018-04-05]. https://pubmed.ncbi.nlm.nih.gov/29618664/. DOI: 10.1172/jci.insight.120157.
18. Wang L, Lee AY, Wigg JP, et al. MiR-126 regulation of angiogenesis in age-related macular degeneration in CNV mouse model[J/OL]. Int J Mol Sci, 2016, 17(6): 895[2016-06-07]. https://pubmed.ncbi.nlm.nih.gov/27338342/. DOI: 10.3390/ijms17060895.
19. Westenskow PD, Kurihara T, Aguilar E, et al. Ras pathway inhibition prevents neovascularization by repressing endothelial cell sprouting[J]. J Clin Invest, 2013, 123(11): 4900-4908. DOI: 10.1172/JCI70230.
20. Nunes DN, Dias-Neto E, Cardó-Vila M, et al. Synchronous down-modulation of miR-17 family members is an early causative event in the retinal angiogenic switch[J]. Proc Natl Acad Sci USA, 2015, 112(12): 3770-3775. DOI: 10.1073/pnas.1500008112.
21. Liu CH, Huang S, BrittonWR, et al. MicroRNAs in vascular eye diseases[J/OL]. Int J Mol Sci, 2020, 21(2): 649[2019-01-19]. https://pubmed.ncbi.nlm.nih.gov/31963809/. DOI: 10.3390/ijms21020649.
22. Blasiak J, Watala C, Tuuminen R, et al. Expression of VEGFA-regulating miRNAs and mortality in wet AMD[J]. J Cell Mol Med, 2019, 23(12): 8464-8471. DOI: 10.1111/jcmm.14731.
23. Elbay A, Ercan Ç, Akbaş F, et al. Three new circulating microRNAs may be associated with wet age-related macular degeneration[J]. Scand J Clin Lab Invest, 2019, 79(6): 388-394. DOI: 10.1080/00365513.2019.1637931.
24. Walz JM, Wecker T, Zhang PP, et al. Impact of angiogenic activation and inhibition on miRNA profiles of human retinal endothelial cells[J]. Exp Eye Res, 2019, 4(181): 98-104. DOI: 10.1016/j.exer.2019.01.006.
25. Lian C, Lou H, Zhang J, et al. MicroRNA-24 protects retina from degeneration in rats by down-regulating chitinase-3-like protein 1[J/OL]. Exp Eye Res, 2019, 9(188): 107791[2019-09-03]. https://pubmed.ncbi.nlm.nih.gov/31491426/. DOI: 10.1016/j.exer.2019.107791.
26. Chu-Tan JA, Rutar M, Saxena K, et al. MicroRNA-124 dysregulation is associated with retinal inflammation and photoreceptor death in the degenerating retina[J]. Invest Ophthalmol Vis Sci, 2018, 59(10): 4094-4105. DOI: 10.1167/iovs.18-24623.
27. Liu J, Ma Z, Ran Z. MiR-21-3p modulates lipopolysaccharide-induced inflammation and apoptosis via targeting TGS 4 in retinal pigment epithelial cells[J]. Clin Exp Pharmacol Physiol, 2019, 46(10): 883-889. DOI: 10.1111/1440-1681.13142.
28. Cheng Y, Du L, Jiao H, et al. Mmu-miR-27a-5p-dependent upregulation of MCPIP1 inhibits the inflammatory response in LPS-induced RAW264.7 macrophage cells[J/OL]. Biomed Res Int, 2015, 2015: 607692[2015-07-30]. https://pubmed.ncbi.nlm.nih.gov/26295043/. DOI: 10.1155/2015/607692.
29. SanGiovanni JP, SanGiovanni PM, Sapieha P, et al. miRNAs, single nucleotide polymorphisms (SNPs) and age-related macular degeneration (AMD)[J]. Clin Chem Lab Med, 2017, 55(5): 763-775. DOI: 10.1515/cclm-2016-0898.
30. Bhattacharjee S, Zhao Y, Dua P, et al. MicroRNA-34a-mediated down-regulation of the microglial-enriched triggering receptor and phagocytosis-sensor TREM2 in age-related macular degeneration[J/OL]. PLoS One, 2016, 11(3): e0150211[2016-03-07]. https://pubmed.ncbi.nlm.nih.gov/26949937/. DOI: 10.1371/journal.pone.0150211.
31. Huang P, Sun J, Wang F, et al. MicroRNA expression patterns involved in amyloid beta-induced retinal degeneration[J]. Invest Ophthalmol Vis Sci, 2017, 58(3): 1726-1735. DOI: 10.1167/iovs.16-20043.
32. To KKW, Fong W, Tong CWS, et al. Advances in the discovery of microRNA-based anticancer therapeutics: latest tools and developments[J]. Expert Opin Drug Discov, 2020, 15(1): 63-83. DOI: 10.1080/17460441.2020.1690449.
33. Askou AL, Alsing S, Benckendorff JNE, et al. Suppression of choroidal neovascularization by AAV-based dual-acting antiangiogenic gene therapy[J]. Mol Ther Nucleic Acids, 2019, 16: 38-50. DOI: 10.1016/j.omtn.2019.01.012.

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