Research progress of microglia in hereditary retinal degeneration_Chinese Journal of Ocular Fundus Diseases

Authors：

Xiang Shengjin ,  Duan Junguo

Academy of Ophthalmology, Chengdu University of Traditional Chinese Medicine, Chengdu 610075, China;

Corresponding author：

Duan Junguo, Email: duanjg@vip.sina.com

Keywords：

Microglia; Eye diseases, hereditary; Review

DOI：

10.3760/cma.j.cn511434-20210331-00165

Video：

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Abstract Full text Figures/Tables Video References Cited by

The human hereditary retinal degeneration is one of the main cause of irreversible blindness in the world. the mechanisms leading to retinal photoreceptor degeneration are not entirely clear. However, microglia acting as innate immune monitors are found to be activated early in retinal degeneration in many retinitis pigmentosa animal models. These activated microglia are involved in phagocyte rod cell fragments of degenerated retina, and also produce high levels of cytotoxic substances such as pro-inflammatory cytokines and chemokines, which aggravate the death of adjacent healthy photoreceptor cells. It suggests that microglia activation plays an important role in photoreceptor degeneration. At the same time, a series of studies have confirmed that some drugs can prevent or reduce neuronal death and slow the occurrence and progression of retinal degeneration by interfering with abnormal activation of microglia. It is expected to be a new choice for the treatment of hereditary retinal degeneration.

Citation： Xiang Shengjin, Duan Junguo. Research progress of microglia in hereditary retinal degeneration. Chinese Journal of Ocular Fundus Diseases, 2022, 38(8): 702-706. doi: 10.3760/cma.j.cn511434-20210331-00165 Copy

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20.	Dannhausen K, Rashid K, Langmann T. Microglia analysis in retinal degeneration mouse models[J]. Methods Mol Biol, 2018, 1753: 159-166. DOI: 10.1007/978-1-4939-7720-8_10.
21.	Silverman SM, Wong WT. Microglia in the retina: roles in development, maturity, and disease[J]. Annu Rev Vis Sci, 2018, 4: 45-77. DOI: 10.1146/annurev-vision-091517-034425.
22.	Yoshida N, Ikeda Y, Notomi S, et al. Laboratory evidence of sustained chronic inflammatory reaction in retinitis pigmentosa[J/OL]. Ophthalmology, 2013, 120(1): e5-12[2012-09-15]. https://pubmed.ncbi.nlm.nih.gov/22986110/. DOI: 10.1016/j.ophtha.2012.07.008.
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24.	Zhao L, Zabel MK, Wang X, et al. Microglial phagocytosis of living photoreceptors contributes to inherited retinal degeneration[J]. EMBO Mol Med, 2015, 7(9): 1179-1197. DOI: 10.15252/emmm.201505298.
25.	Wang NK, Lai CC, Liu CH, et al. Origin of fundus hyperautofluorescent spots and their role in retinal degeneration in a mouse model of Goldmann-Favre syndrome[J]. Dis Model Mech, 2013, 6(5): 1113-1122. DOI: 10.1242/dmm.012112.
26.	Aredo B, Zhang K, Chen X, et al. Differences in the distribution, phenotype and gene expression of subretinal microglia/macrophages in C57BL/6N (Crb1 rd8/rd8) versus C57BL6/J (Crb1 wt/wt) mice[J]. J Neuroinflammation, 2015, 12: 6. DOI: 10.1186/s12974-014-0221-4.
27.	Langmann T, Ebert S, Walczak Y, et al. Induction of early growth response-1 mediates microglia activation in vitro but is dispensable in vivo[J]. Neuromolecular Med, 2009, 11(2): 87-96. DOI: 10.1007/s12017-009-8061-6.
28.	Zhang S, Zhang S, Zhu G, et al. Müller cell regulated microglial activation and migration in rats with N-Methyl-N-Nitrosourea-induced retinal degeneration[J]. Front Neurosci, 2018, 12: 890. DOI: 10.3389/fnins.2018.00890.
29.	Di Pierdomenico J, García-Ayuso D, Pinilla I, et al. Early events in retinal degeneration caused by rhodopsin mutation or pigment epithelium malfunction: differences and similarities[J]. Front Neuroanat, 2017, 11: 14. DOI: 10.3389/fnana.2017.00014.
30.	Guo C, Otani A, Oishi A, et al. Knockout of ccr2 alleviates photoreceptor cell death in a model of retinitis pigmentosa[J]. Exp Eye Res, 2012, 104: 39-47. DOI: 10.1016/j.exer.2012.08.013.
31.	Kohno H, Chen Y, Kevany BM, et al. Photoreceptor proteins initiate microglial activation via Toll-like receptor 4 in retinal degeneration mediated by all-trans-retinal[J]. J Biol Chem, 2013, 288: 15326-15341. DOI: 10.1074/jbc.M112.448712.
32.	Scholz R, Caramoy A, Bhuckory M, et al. Targeting translocator protein (18kDa) (TSPO) dampens pro-inflammatory microglia reactivity in the retina and protects from degeneration[J]. J Neuroinflammation, 2015, 12: 201. DOI: 10.1186/s12974-015-0422-5.
33.	Mages K, Grassmann F, Jägle H, et a1. The agonistic TSPO 1igand XBD173 attenuates the glial response thereby protecting inner retinal neurons in a murine model of retinal ischemia[J]. J Neuroinflammation, 2019, 16(11): 43. DOI: 10.1186/s12974-019-1424-5.
34.	Garrido-Mesa N, Zarzuelo A, Gálvez J. Minocycline: far beyond an antibiotic[J]. Br J Pharmacol, 2013, 169(2): 337-352. DOI: 10.1111/bph.12139.
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36.	Kobayashi K, Imagama S, Ohgomori T, et al. Minocycline selectively inhibits M1 polarization of microglia[J/OL]. Cell Death Dis, 2013, 4(3): e525[2013-03-07]. https://pubmed.ncbi.nlm.nih.gov/23470532/. DOI: 10.1038/cddis.2013.54.
37.	Scholz R, Sobotka M, Caramoy A. Minocycline counter-regulates pro-inflammatory microglia responses in the retina and protects from degeneration[J]. J Neuroinflammation, 2015, 12: 209. DOI: 10.1186/s12974-015-0431-4.
38.	Peng B, Xiao J, Wang K, et al. Suppression of microglial activation is neuroprotective in a mouse model of human retinitis pigmentosa[J]. J Neurosci, 2014, 34(24): 8139-8150. DOI: 10.1523/JNEUROSCI.5200-13.2014.
39.	Cukras CA, Petrou P, Chew EY, et al. Oral minocycline for the treatment of diabetic macular edema (DME): results of a phase Ⅰ/Ⅱ clinical study[J]. Invest Opthalmol Vis Sci, 2012, 53(7): 3865-3874. DOI: 10.1167/iovs.11-9413.
40.	Baumgartner WA, Baumgartner AM. Rationale for an experimental treatment of retinitis pigmentosa: 140-month test of hypothesis with one patient[J]. Med Hypotheses, 2013, 81(4): 720-728. DOI: 10.1016/j.mehy.2013.07.036.
41.	Karali M, Guadagnino I, Marrocco E, et al. AAV-miR-204 protects from retinal degeneration by attenuation of microglia activation and photoreceptor cell death[J]. Mol Ther Nucleic Acids, 2020, 19: 144-156. DOI: 10.1016/j.omtn.2019.11.005.
42.	Wang SK, Xue Y, Cepko CL. Microglia modulation by TGF-β1 protects cones in mouse models of retinal degeneration[J]. J Clin Invest, 2020, 130(8): 4360-4369. DOI: 10.1172/JCI136160.
43.	Tanaka M, Kuse Y, Nakamura S, et al. Potential effects of progranulin and granulins against retinal photoreceptor cell degeneration[J]. Mol Vis, 2019, 25: 902-911.
44.	Zhou T, Huang Z, Zhu X, et al. Alpha-1 antitrces M1 microglia-mediated neuroinflammation in retinal degeneration[J/OL]. Front Immunol, 2018, 9: 1202[2018-05-30]. https://pubmed.ncbi.nlm.nih.gov/29899745/. DOI: 10.3389/fimmu.2018.01202.
45.	Wang Y, Yin Z, Gao L, et al. Curcumin delays retinal degeneration by regulating microglia activation in the retina of rd 1 mice[J]. Cell Physiol Biochem, 2017, 44(2): 479-493. DOI: 10.1159/000485085.
46.	Chumsakul O, Wakayama K, Tsuhako A, et al. Apigenin regulates activation of microglia and counteracts retinal degeneration[J]. J Ocul Pharmacol Ther, 2020, 36(5): 311-319. DOI: 10.1089/jop.2019.0163.

1. Mitamura Y, Mitamura-Aizawa S, Nagasawa T, et al. Diagnostic imaging in patients with retinitis pigmentosa[J]. J Med Invest, 2012, 59(1-2): 1-11. DOI: 10.2152/jmi.59.1.
2. Rashid K, Akhtar-Schaefer I, Langmann T. Microglia in retinal degeneration[J/OL]. Front Immunol, 2019, 10: 1975[2019-08-20]. https://pubmed.ncbi.nlm.nih.gov/31481963/. DOI: 10.3389/fimmu.2019.01975.
3. Karlstetter M, Scholz R, Rutar M, et al. Retinal microglia: just bystander or target for therapy?[J]. Prog Retin Eye Res, 2015, 45: 30-57. DOI: 10.1016/j.preteyeres.2014.11.004.
4. Ramirez AI, de Hoz R, Salobrar-Garcia E, et al. The role of microglia in retinal neurodegeneration: Alzheimer's disease, Parkinson, and Glaucoma[J]. Front Aging Neurosci, 2017, 9: 214. DOI: 10.3389/fnagi.2017.00214.
5. Gupta N, Shyamasundar S, Patnala R, et al. Recent progress in therapeutic strategies for microglia-mediated neuroinflammation in neuropathologies[J]. Expert Opin Ther Targets, 2018, 22(9): 765-781. DOI: 10.1080/14728222.2018.1515917.
6. Bellver-Landete V, Bretheau F, Mailhot B, et al. Microglia are an essential component of the neuroprotective scar that forms after spinal cord injury[J]. Nat Commun, 2019, 10(1): 518. DOI: 10.1038/s41467-019-08446-0.
7. Colonna M, Butovsky O. Microglia function in the central nervous system during health and neurodegeneration[J]. Annu Rev Immunol, 2017, 35: 441-468. DOI: 10.1146/annurev-immunol-051116-052358.
8. Brown GC, Neher JJ. Microglial phagocytosis of live neurons[J]. Nat Rev Neurosci, 2014, 15(4): 209-216. DOI: 10.1038/nrn3710.
9. Tang Y, and Le W. Differential roles of M1 and M2 microglia in neurodegenerative diseases[J]. Mol Neurobiol, 2016, 53(2): 1181-1194. DOI: 10.1007/s12035-014-9070-5.
10. Orihuela R, Mcpherson CA, Harry GJ. Microglial M1/M2 polarization and metabolic states[J]. Br J Pharmacol, 2016, 173(4): 649-665. DOI: 10.1111/bph.13139.
11. Vecino E, Rodriguez FD, Ruzafa N, et al. Glia-neuron interactions in the mammalian retina[J]. Prog Retin Eye Res, 2016, 51: 1-40. DOI: 10.1016/j.preteyeres.2015.06.003.
12. Wolf Y, Yona S, Kim KW, et al. Microglia, seen from the CX3CR1 angle[J]. Front Cell Neurosci, 2013, 7: 26. DOI: 10.3389/fncel.2013.00026.
13. Zabel MK, Zhao L, Zhang Y, et al. Microglial phagocytosis and activation underlying photoreceptor degeneration is regulated by CX3CL1-CX3CR1 signaling in a mouse model of retinitis pigmentosa[J]. Glia, 2016, 64(9): 1479-1491. DOI: 10.1002/glia.23016.
14. Horie S, Robbie SJ, Liu J, et al. CD200R signaling inhibits pro-angiogenic gene expression by macrophages and suppresses choroidal neovascularization[J/OL]. Sci Rep, 2013, 3: 3072[2013-10-30]. https://pubmed.ncbi.nlm.nih.gov/24170042/. DOI: 10.1038/srep03072.
15. Rashid K, Verhoyen M, Taiwo M, et al. Translocator protein (18 kDa) (TSPO) ligands activate Nrf2 signaling and attenuate inflammatory responses and oxidative stress in human retinal pigment epithelial cells[J]. Biochem Biophys Res Commun, 2020, 528(2): 261-268. DOI: 10.1016/j.bbrc.2020.05.114.
16. Madeira MH, Boia R, Santos PF, et al. Contribution of microglia-mediated neuroinflammation to retinal degenerative diseases[J/OL]. Mediators Inflamm, 2015, 2015: 673090[2015-03-22]. https://pubmed.ncbi.nlm.nih.gov/25873768/. DOI: 10.1155/2015/673090.
17. Wang M, Ma W, Zhao L, et al. Adaptive Müller cell responses to microglial activation mediate neuroprotection and coordinate inflammation in the retina[J]. J Neuroinflammation, 2011, 8: 173. DOI: 10.1186/1742-2094-8-173.
18. Wang M, Wang X, Zhao L, et al. Macroglia-microglia interactions via TSPO signaling regulates microglial activation in the mouse retina[J]. J Neurosci, 2014, 34: 3793-3806. DOI: 10.1523/JNEUROSCI.3153-13.2014.
19. Di Pierdomenico J, García-Ayuso D, Agudo-Barriuso M, et al. Role of microglial cells in photoreceptor degeneration[J]. Neural Regen Res, 2019, 14(7): 1186-1190. DOI: 10.4103/1673-5374.251204.
20. Dannhausen K, Rashid K, Langmann T. Microglia analysis in retinal degeneration mouse models[J]. Methods Mol Biol, 2018, 1753: 159-166. DOI: 10.1007/978-1-4939-7720-8_10.
21. Silverman SM, Wong WT. Microglia in the retina: roles in development, maturity, and disease[J]. Annu Rev Vis Sci, 2018, 4: 45-77. DOI: 10.1146/annurev-vision-091517-034425.
22. Yoshida N, Ikeda Y, Notomi S, et al. Laboratory evidence of sustained chronic inflammatory reaction in retinitis pigmentosa[J/OL]. Ophthalmology, 2013, 120(1): e5-12[2012-09-15]. https://pubmed.ncbi.nlm.nih.gov/22986110/. DOI: 10.1016/j.ophtha.2012.07.008.
23. Blank T, Goldmann T, Koch M, et al. Early microglia activation precedes photoreceptor degeneration in a mouse model of CNGB1-linked retinitis pigmentosa[J/OL]. Front Immunol, 2018, 8: 1930[2018-01-05]. https://pubmed.ncbi.nlm.nih.gov/29354133/. DOI: 10.3389/fimmu.2017.01930.
24. Zhao L, Zabel MK, Wang X, et al. Microglial phagocytosis of living photoreceptors contributes to inherited retinal degeneration[J]. EMBO Mol Med, 2015, 7(9): 1179-1197. DOI: 10.15252/emmm.201505298.
25. Wang NK, Lai CC, Liu CH, et al. Origin of fundus hyperautofluorescent spots and their role in retinal degeneration in a mouse model of Goldmann-Favre syndrome[J]. Dis Model Mech, 2013, 6(5): 1113-1122. DOI: 10.1242/dmm.012112.
26. Aredo B, Zhang K, Chen X, et al. Differences in the distribution, phenotype and gene expression of subretinal microglia/macrophages in C57BL/6N (Crb1 rd8/rd8) versus C57BL6/J (Crb1 wt/wt) mice[J]. J Neuroinflammation, 2015, 12: 6. DOI: 10.1186/s12974-014-0221-4.
27. Langmann T, Ebert S, Walczak Y, et al. Induction of early growth response-1 mediates microglia activation in vitro but is dispensable in vivo[J]. Neuromolecular Med, 2009, 11(2): 87-96. DOI: 10.1007/s12017-009-8061-6.
28. Zhang S, Zhang S, Zhu G, et al. Müller cell regulated microglial activation and migration in rats with N-Methyl-N-Nitrosourea-induced retinal degeneration[J]. Front Neurosci, 2018, 12: 890. DOI: 10.3389/fnins.2018.00890.
29. Di Pierdomenico J, García-Ayuso D, Pinilla I, et al. Early events in retinal degeneration caused by rhodopsin mutation or pigment epithelium malfunction: differences and similarities[J]. Front Neuroanat, 2017, 11: 14. DOI: 10.3389/fnana.2017.00014.
30. Guo C, Otani A, Oishi A, et al. Knockout of ccr2 alleviates photoreceptor cell death in a model of retinitis pigmentosa[J]. Exp Eye Res, 2012, 104: 39-47. DOI: 10.1016/j.exer.2012.08.013.
31. Kohno H, Chen Y, Kevany BM, et al. Photoreceptor proteins initiate microglial activation via Toll-like receptor 4 in retinal degeneration mediated by all-trans-retinal[J]. J Biol Chem, 2013, 288: 15326-15341. DOI: 10.1074/jbc.M112.448712.
32. Scholz R, Caramoy A, Bhuckory M, et al. Targeting translocator protein (18kDa) (TSPO) dampens pro-inflammatory microglia reactivity in the retina and protects from degeneration[J]. J Neuroinflammation, 2015, 12: 201. DOI: 10.1186/s12974-015-0422-5.
33. Mages K, Grassmann F, Jägle H, et a1. The agonistic TSPO 1igand XBD173 attenuates the glial response thereby protecting inner retinal neurons in a murine model of retinal ischemia[J]. J Neuroinflammation, 2019, 16(11): 43. DOI: 10.1186/s12974-019-1424-5.
34. Garrido-Mesa N, Zarzuelo A, Gálvez J. Minocycline: far beyond an antibiotic[J]. Br J Pharmacol, 2013, 169(2): 337-352. DOI: 10.1111/bph.12139.
35. Halder SK, Matsunaga H, Ishii KJ, et al. Retinal cell type-specific prevention of ischemia-induced damages by LPS-TLR4 signaling through microglia[J]. J Neurochem, 2013, 126(2): 243-260. DOI: 10.1111/jnc.12262.
36. Kobayashi K, Imagama S, Ohgomori T, et al. Minocycline selectively inhibits M1 polarization of microglia[J/OL]. Cell Death Dis, 2013, 4(3): e525[2013-03-07]. https://pubmed.ncbi.nlm.nih.gov/23470532/. DOI: 10.1038/cddis.2013.54.
37. Scholz R, Sobotka M, Caramoy A. Minocycline counter-regulates pro-inflammatory microglia responses in the retina and protects from degeneration[J]. J Neuroinflammation, 2015, 12: 209. DOI: 10.1186/s12974-015-0431-4.
38. Peng B, Xiao J, Wang K, et al. Suppression of microglial activation is neuroprotective in a mouse model of human retinitis pigmentosa[J]. J Neurosci, 2014, 34(24): 8139-8150. DOI: 10.1523/JNEUROSCI.5200-13.2014.
39. Cukras CA, Petrou P, Chew EY, et al. Oral minocycline for the treatment of diabetic macular edema (DME): results of a phase Ⅰ/Ⅱ clinical study[J]. Invest Opthalmol Vis Sci, 2012, 53(7): 3865-3874. DOI: 10.1167/iovs.11-9413.
40. Baumgartner WA, Baumgartner AM. Rationale for an experimental treatment of retinitis pigmentosa: 140-month test of hypothesis with one patient[J]. Med Hypotheses, 2013, 81(4): 720-728. DOI: 10.1016/j.mehy.2013.07.036.
41. Karali M, Guadagnino I, Marrocco E, et al. AAV-miR-204 protects from retinal degeneration by attenuation of microglia activation and photoreceptor cell death[J]. Mol Ther Nucleic Acids, 2020, 19: 144-156. DOI: 10.1016/j.omtn.2019.11.005.
42. Wang SK, Xue Y, Cepko CL. Microglia modulation by TGF-β1 protects cones in mouse models of retinal degeneration[J]. J Clin Invest, 2020, 130(8): 4360-4369. DOI: 10.1172/JCI136160.
43. Tanaka M, Kuse Y, Nakamura S, et al. Potential effects of progranulin and granulins against retinal photoreceptor cell degeneration[J]. Mol Vis, 2019, 25: 902-911.
44. Zhou T, Huang Z, Zhu X, et al. Alpha-1 antitrces M1 microglia-mediated neuroinflammation in retinal degeneration[J/OL]. Front Immunol, 2018, 9: 1202[2018-05-30]. https://pubmed.ncbi.nlm.nih.gov/29899745/. DOI: 10.3389/fimmu.2018.01202.
45. Wang Y, Yin Z, Gao L, et al. Curcumin delays retinal degeneration by regulating microglia activation in the retina of rd 1 mice[J]. Cell Physiol Biochem, 2017, 44(2): 479-493. DOI: 10.1159/000485085.
46. Chumsakul O, Wakayama K, Tsuhako A, et al. Apigenin regulates activation of microglia and counteracts retinal degeneration[J]. J Ocul Pharmacol Ther, 2020, 36(5): 311-319. DOI: 10.1089/jop.2019.0163.

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