Biochemistry (Moscow)

, Volume 83, Issue 9, pp 1009–1017 | Cite as

Changes in Retinal Glial Cells with Age and during Development of Age-Related Macular Degeneration

  • D. V. Telegina
  • O. S. Kozhevnikova
  • N. G. KolosovaEmail author


Age is the major risk factor in the age-related macular degeneration (AMD) which is a complex multifactor neurodegenerative disease of the retina and the main cause of irreversible vision loss in people over 60 years old. The major role in AMD pathogenesis belongs to structure-functional changes in the retinal pigment epithelium cells, while the onset and progression of AMD are commonly believed to be caused by the immune system dysfunctions. The role of retinal glial cells (Muller cells, astrocytes, and microglia) in AMD pathogenesis is studied much less. These cells maintain neurons and retinal vessels through the synthesis of neurotrophic and angiogenic factors, as well as perform supporting, separating, trophic, secretory, and immune functions. It is known that retinal glia experiences morphological and functional changes with age. Age-related impairments in the functional activity of glial cells are closely related to the changes in the expression of trophic factors that affect the status of all cell types in the retina. In this review, we summarized available literature data on the role of retinal macro- and microglia and on the contribution of these cells to AMD pathogenesis.


aging retina age-related macular degeneration astrocytes Muller cells microglia 



age-related macular degeneration


C-X3-C-motif of chemokine receptor 1


glial fibrillar acidic protein




retinal pigment epithelium


tumor necrosis factor


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Shao, J., Choudhary, M. M., and Schachat, A. P. (2016) Neovascular age-related macular degeneration, in Retinal Pharmacotherapeutics, Karger Publishers, Vol. 55, pp. 125–136.Google Scholar
  2. 2.
    Telegina, D. V., Kozhevnikova, O. S., and Kolosova, N. G. (2017) Molecular mechanisms of cell death in retina during development of age-related macular degeneration, Adv. Gerontol., 7, 17–24.CrossRefGoogle Scholar
  3. 3.
    Ardeljan, D., and Chan, C. C. (2013) Aging is not a disease: distinguishing age-related macular degeneration from aging, Prog. Retin. Eye Res., 37, 68–89.CrossRefPubMedGoogle Scholar
  4. 4.
    Cuenca, N., Fernandez-Sanchez, L., Campello, L., Maneu, V., De la Villa, P., Lax, P., and Pinilla, I. (2014) Cellular responses following retinal injuries and therapeutic approaches for neurodegenerative diseases, Prog. Retin. Eye Res., 43, 17–75.CrossRefPubMedGoogle Scholar
  5. 5.
    Bora, N. S., Matta, B., Lyzogubov, V. V., and Bora, P. S. (2015) Relationship between the complement system, risk factors and prediction models in age-related macular degeneration, Mol. Immunol., 63, 176–183.CrossRefPubMedGoogle Scholar
  6. 6.
    Goldman, D. (2014) Muller glial cell reprogramming and retina regeneration, Nat. Rev. Neurosci., 15, 431–442.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Coorey, N. J., Shen, W., Chung, S. H., Zhu, L., and Gillies, M. C. (2012) The role of glia in retinal vascular disease, Clin. Exp. Optometry, 95, 266–281.CrossRefGoogle Scholar
  8. 8.
    Rossi, D. (2015) Astrocyte physiopathology: at the cross-roads of intercellular networking, inflammation and cell death, Prog. Neurobiol., 130, 86–120.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Kur, J., Newman, E. A., and Chan-Ling, T. (2012) Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease, Prog. Retin. Eye Res., 31, 377–406.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Vecino, E., Rodriguez, F. D., Ruzafa, N., Pereiro, X., and Sharma, S. C. (2016) Glia-neuron interactions in the mammalian retina, Prog. Retin. Eye Res., 51, 1–40.CrossRefPubMedGoogle Scholar
  11. 11.
    Newman, E. A. (2015) Glial cell regulation of neuronal activity and blood flow in the retina by release of gliotransmitters, Phil. Trans. R. Soc. B, 370, 20140195.CrossRefPubMedGoogle Scholar
  12. 12.
    De Hoz, R., Rojas, B., Ramirez, A. I., Salazar, J. J., Gallego, B. I., Trivino, A., and Ramirez, J. M. (2016) Retinal macroglial responses in health and disease, BioMed. Res. Int., 2016, 2954721.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Kim, J. H., Kim, J. H., Park, J., Lee, S. W., Kim, W. J., Yu, Y. S., and Kim, K. W. (2006) Blood-neural barrier: intercellular communication at glio-vascular interface, J. Biochem. Mol. Biol., 39, 339–345.PubMedGoogle Scholar
  14. 14.
    Zhang, X., Cheng, M., and Chintala, S. K. (2004) Kainic acid-mediated upregulation of matrix metalloproteinase-9 promotes retinal degeneration, Invest. Ophthalm. Vis. Sci., 45, 2374–2383.CrossRefGoogle Scholar
  15. 15.
    Ramirez, J. M., Ramirez, A. I., Salazar, J. J., de Hoz, R., and Trivino, A. (2001) Changes of astrocytes in retinal ageing and age-related macular degeneration, Exp. Eye Res., 73, 601–615.CrossRefPubMedGoogle Scholar
  16. 16.
    Jadhav, A. P., Cho, S. H., and Cepko, C. L. (2006) Notch activity permits retinal cells to progress through multiple progenitor states and acquire a stem cell property, Proc. Natl. Acad. Sci. USA, 103, 18998–19003.CrossRefPubMedGoogle Scholar
  17. 17.
    Jadhav, A. P., Roesch, K., and Cepko, C. L. (2009) Development and neurogenic potential of Muller glial cells in the vertebrate retina, Prog. Retin. Eye Res., 28, 249–262.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Goureau, O., Do Rhee, K., and Yang, X. J. (2004) Ciliary neurotrophic factor promotes Muller glia differentiation from the postnatal retinal progenitor pool, Dev. Neurosci., 26, 359–370.CrossRefPubMedGoogle Scholar
  19. 19.
    Bhattacharya, S., Das, A. V., Mallya, K. B., and Ahmad, I. (2008) Ciliary neurotrophic factor-mediated signaling regulates neuronal versus glial differentiation of retinal stem cell/progenitors by concentration-dependent recruitment of mitogens-activated protein kinase and Janus kinase-signal transducer and activator of transcription pathways in conjunction with Notch signaling, Stem Cells, 26, 2611–2624.CrossRefPubMedGoogle Scholar
  20. 20.
    Dubois-Dauphin, M., Poitry-Yamate, C., De Bilbao, F., Julliard, A. K., Jourdan, F., and Donati, G. (1999) Early postnatal Muller cell death leads to retinal but not optic nerve degeneration in NSE-Hu-Bcl-2 transgenic mice, Neuroscience, 95, 9–21.CrossRefGoogle Scholar
  21. 21.
    Xia, X., and Ahmad, I. (2016) Unlocking the neurogenic potential of mammalian Muller glia, Int. J. Stem Cells, 9, 169–175.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Hamon, A., Roger, J. E., Yang, X. J., and Perron, M. (2016) Muller glial cell-dependent regeneration of the neural retina: an overview across vertebrate model systems, Develop. Dynam., 245, 727–738.CrossRefGoogle Scholar
  23. 23.
    Webster, M. K., Cooley-Themm, C., Barnett, J. D., Bach, H. B., Vainner, J. M., Webster, S. E., and Linn, C. L. (2017) Evidence of BrdU-positive retinal neurons after application of an Alpha7 nicotinic acetylcholine receptor agonist, Neuroscience, 346, 437–446.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Bringmann, A., and Wiedemann, P. (2012) Muller glial cells in retinal disease, Ophthalmologica, 227, 1–19.CrossRefPubMedGoogle Scholar
  25. 25.
    Gallina, D., Todd, L., and Fischer, A. J. (2014) A comparative analysis of Muller glia-mediated regeneration in the vertebrate retina, Exp. Eye Res., 123, 121–130.CrossRefPubMedGoogle Scholar
  26. 26.
    Kolomeyer, A. M., and Zarbin, M. A. (2014) Trophic factors in the pathogenesis and therapy for retinal degenerative diseases, Survey Ophthalmol., 59, 134–165.CrossRefGoogle Scholar
  27. 27.
    Hurley, J. B., Chertov, A. O., Lindsay, K., Giamarco, M., Cleghorn, W., Du, J., and Brockerhoff, S. (2014) Energy metabolism in the vertebrate retina, in Vertebrate Photoreceptors, Springer, Japan, pp. 91–137.CrossRefGoogle Scholar
  28. 28.
    Reichenbach, A., and Bringmann, A. (2013) New functions of Muller cells, Glia, 61, 651–678.CrossRefPubMedGoogle Scholar
  29. 29.
    Schey, K. L., Wang, Z., Wenke, J. L., and Qi, Y. (2014) Aquaporins in the eye: expression, function, and roles in ocular disease, Biochim. Biophys. Acta, 1840, 1513–1523.CrossRefPubMedGoogle Scholar
  30. 30.
    Hippert, C., Graca, A. B., Barber, A. C., West, E. L., Smith, A. J., Ali, R. R., and Pearson, R. A. (2015) Muller glia activation in response to inherited retinal degeneration is highly varied and disease-specific, PLoS One, 10, e0120415.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Luna, G., Lewis, G. P., Banna, C. D., Skalli, O., and Fisher, S. K. (2010) Expression profiles of nestin and synemin in reactive astrocytes and Muller cells following retinal injury: a comparison with glial fibrillar acidic protein and vimentin, Mol. Vis., 16, 2511–2523.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Belecky-Adams, T. L., Chernoff, E. C., Wilson, J. M., and Dharmarajan, S. (2013) Reactive Muller glia as potential retinal progenitors, in Neural Stem Cells-New Perspectives, InTech.Google Scholar
  33. 33.
    Hol, E. M., and Pekny, M. (2015) Glial fibrillary acidic protein (GFAP) and the astrocyte intermediate filament system in diseases of the central nervous system, Curr. Opin. Cell Biol., 32, 121–130.CrossRefPubMedGoogle Scholar
  34. 34.
    Nakazawa, T., Takeda, M., Lewis, G. P., Cho, K. S., Jiao, J., Wilhelmsson, U., Fisher, S. K., Pekny, M., Chen, D. F., and Miller, J. W. (2007) Attenuated glial reactions and photoreceptor degeneration after retinal detachment in mice deficient in glial fibrillary acidic protein and vimentin, Invest. Ophthalmol. Vis. Sci., 48, 2760–2768.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Edwards, M. M., McLeod, D. S., Bhutto, I. A., Villalonga, M. B., Seddon, J. M., and Lutty, G. A. (2016) Idiopathic preretinal glia in aging and age-related macular degeneration, Exp. Eye Res., 150, 44–61.CrossRefPubMedGoogle Scholar
  36. 36.
    Verkhratsky, A., Rodriguez, J. J., and Parpura, V. (2014) Neuroglia in ageing and disease, Cell Tissue Res., 357, 493–503.CrossRefPubMedGoogle Scholar
  37. 37.
    Ganesh, B. S., and Chintala, S. K. (2011) Inhibition of reactive gliosis attenuates excitotoxicity-mediated death of retinal ganglion cells, PloS One, 6, e18305.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Kalloniatis, M., Nivison-Smith, L., Chua, J., Acosta, M. L., and Fletcher, E. L. (2016) Using the rd1 mouse to understand functional and anatomical retinal remodelling and treatment implications in retinitis pigmentosa: a review, Exp. Eye Res., 150, 106–121.CrossRefPubMedGoogle Scholar
  39. 39.
    Telegina, D. V., Kozhevnikova, O. S., Bayborodin, S. I., and Kolosova, N. G. (2017) Contributions of age-related alterations of the retinal pigment epithelium and of glia to the AMD-like pathology in OXYS rats, Sci. Rep., 7, 41533.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Kozhevnikova, O. S., Telegina, D. V., Devyatkin, V. A., and Kolosova, N. G. (2018) Involvement of the autophagic path-way in the progression of AMD-like retinopathy in senes-cence-accelerated OXYS rats, Biogerontology, 19, 223–235.CrossRefPubMedGoogle Scholar
  41. 41.
    Telegina, D. V., Korbolina, E. E., Ershov, N. I., Kolosova, N. G., and Kozhevnikova, O. S. (2015) Identification of functional networks associated with cell death in the retina of OXYS rats during the development of retinopathy, Cell Cycle, 14, 3544–3556.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Kettenmann, H., Hanisch, U. K., Noda, M., and Verkhratsky, A. (2011) Physiology of microglia, Physiol. Rev., 91, 461–553.CrossRefPubMedGoogle Scholar
  43. 43.
    Ohsawa, K., Imai, Y., Sasaki, Y., and Kohsaka, S. (2004) Microglia/macrophage-specific protein Iba1 binds to fibrin and enhances its actin-binding activity, J. Neurochem., 88, 844–856.CrossRefPubMedGoogle Scholar
  44. 44.
    Langmann, T. (2007) Microglia activation in retinal degeneration, J. Leukoc. Biol., 81, 1345–1351.CrossRefPubMedGoogle Scholar
  45. 45.
    Nimmerjahn, A., Kirchhoff, F., and Helmchen, F. (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo, Science, 308, 1314–1318.CrossRefPubMedGoogle Scholar
  46. 46.
    Fu, R., Shen, Q., Xu, P., Luo, J. J., and Tang, Y. (2014) Phagocytosis of microglia in the central nervous system diseases, Mol. Neurobiol., 49, 1422–1434.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Xu, H., Chen, M., and Forrester, J. V. (2009) Para-inflammation in the aging retina, Progr. Retin. Eye Res., 28, 348–368.CrossRefGoogle Scholar
  48. 48.
    Karlstetter, M., Scholz, R., Rutar, M., Wong, W. T., Provis, J. M., and Langmann, T. (2015) Retinal microglia: just bystander or target for therapy? Prog. Retin. Eye Res., 45, 30–57.CrossRefPubMedGoogle Scholar
  49. 49.
    Perry, V. H., and Teeling, J. (2013) Microglia and macrophages of the central nervous system: the contribution of microglia priming and systemic inflammation to chronic neurodegeneration, Semin. Immunopathol., 35, 601–612.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Paglinawan, R., Malipiero, U., Schlapbach, R., Frei, K., Reith, W., and Fontana, A. (2003) TGFβ directs gene expression of activated microglia to an anti-inflammatory phenotype strongly focusing on chemokines genes and cell migratory genes, Glia, 44, 219–231.CrossRefPubMedGoogle Scholar
  51. 51.
    Karlstetter, M., Nothdurfter, C., Aslanidis, A., Moeller, K., Horn, F., Scholz, R., Neumann, H., Weber, B. H., Rupprecht, R., and Langmann, T. (2014) Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis, J. Neuroinflamm., 11,3.CrossRefGoogle Scholar
  52. 52.
    Wang, M., Wang, X., Zhao, L., Ma, W., Rodriguez, I. R., Fariss, R. N., and Wong, W. T. (2014) Macroglia-microglia interactions via TSPO signaling regulates microglial activation in the mouse retina, J. Neurosci., 34, 3793–3806.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Kimura, A., Namekata, K., Guo, X., Harada, C., and Harada, T. (2016) Neuroprotection, growth factors and BDNF-TrkB signalling in retinal degeneration, Int. J. Mol. Sci., 17, E1584.CrossRefPubMedGoogle Scholar
  54. 54.
    Cardona, A. E., Pioro, E. P., Sasse, M. E., Kostenko, V., Cardona, S. M., Dijkstra, I. M., Huang, D., Kidd, G., Dombrowski, S., Dutta, R., Lee, J. C., Cook, D. N., Jung, S., Lira, S. A., Littman, D. R., and Ransohoff, R. M. (2006) Control of microglial neurotoxicity by the fractalkine receptor, Nat. Neurosci., 9, 917–924.CrossRefPubMedGoogle Scholar
  55. 55.
    Liang, K. J., Lee, J. E., Wang, Y. D., Ma, W., Fontainhas, A. M., Fariss, R. N., and Wong, W. T. (2009) Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling, Invest. Ophthalmol. Vis. Sci., 50, 4444–4451.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Sheridan, G. K., and Murphy, K. J. (2013) Neuronglia crosstalk in health and disease: fractalkine and CX3CR1 take centre stage, Open Biol., 3, 130181.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Damani, M. R., Zhao, L., Fontainhas, A. M., Amaral, J., Fariss, R. N., and Wong, W. T. (2011) Age-related alterations in the dynamic behavior of microglia, Aging Cells, 10, 263–276.CrossRefGoogle Scholar
  58. 58.
    Ma, W., Coon, S., Zhao, L., Fariss, R. N., and Wong, W. T. (2013) A2E accumulation influences retinal microglial activation and complement regulation, Neurobiol. Aging, 34, 943–960.CrossRefPubMedGoogle Scholar
  59. 59.
    Ma, W., and Wong, W. T. (2016) Aging changes in retinal microglia and their relevance to age-related retinal disease, Adv. Exp. Med. Biol., 854, 73–78.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Medzhitov, R. (2008) Origin and physiological roles of inflammation, Nature, 454, 428–435.CrossRefPubMedGoogle Scholar
  61. 61.
    Karlstetter, M., Ebert, S., and Langmann, T. (2010) Microglia in the healthy and degenerating retina: insights from novel mouse models, Immunobiology, 215, 685–691.CrossRefPubMedGoogle Scholar
  62. 62.
    Polazzi, E., and Monti, B. (2010) Microglia and neuroprotection: from in vitro studies to therapeutic applications, Progr. Neurobiol., 92, 293–315.CrossRefGoogle Scholar
  63. 63.
    Gupta, N., Brown, K. E., and Milam, A. H. (2003) Activated microglia in human retinitis pigmentosa, lateonset retinal degeneration, and age–related macular degeneration, Exp. Eye Res., 76, 463–471.CrossRefPubMedGoogle Scholar
  64. 64.
    Luhmann, U. F., Lange, C. A., Robbie, S., Munro, P. M., Cowing, J. A., Armer, H. E., Luong, V., Carvalho, L. S., MacLaren, R. E., Fitzke, F. W., Bainbridge, J. W., and Ali, R. R. (2012) Differential modulation of retinal degeneration by Ccl2 and Cx3cr1 chemokine signaling, PLoS One, 7, e35551.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Hollyfield, J. G., Bonilha, V. L., Rayborn, M. E., Yang, X., Shadrach, K. G., Lu, L., Ufret, R. L., Salomon, R. G., and Perez, V. L. (2008) Oxidative damage-induced inflammation initiates age-related macular degeneration, Nat. Med., 14, 194–198.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Hollyfield, J. G., Perez, V. L., and Salomon, R. G. (2010) A hapten generated from an oxidation fragment of docosahexaenoic acid is sufficient to initiate age-related macular degeneration, Mol. Neurobiol., 41, 290–298.CrossRefPubMedGoogle Scholar
  67. 67.
    Cruz-Guilloty, F., Saeed, A. M., Echegaray, J. J., Duffort, S., Ballmick, A., Tan, Y., Betancourt, M., Viteri, E., Ramkhellawan, G. C., Ewald, E., Feuer, W., Huang, D., Wen, R., Hong, L., Wang, H., Laird, J. M., Sene, A., Apte, R. S., Salomon, R. G., Hollyfield, J. G., and Perez, V. L. (2013) Infiltration of proinflammatory m1 macrophages into the external retina precedes damage in a mouse model of age-related macular degeneration, Int. J. Inflamm., 2013, 503725.CrossRefGoogle Scholar
  68. 68.
    Ufret-Vincenty, R. L., Aredo, B., Liu, X., McMahon, A., Chen, P. W., Sun, H., Niederkorn, J. Y., and Kedzierski, W. (2010) Transgenic mice expressing variants of complement factor H develop AMD-like retinal findings, Invest. Ophthalmol. Vis. Sci., 51, 5878–5887.CrossRefPubMedGoogle Scholar
  69. 69.
    Combadiere, C., Feumi, C., Raoul, W., Keller, N., Rodero, M., Pezard, A., Lavalette, S., Houssier, M., Jonet, L., Picard, E., Debre, P., Sirinyan, M., Deterre, P., Ferroukhi, T., Cohen, S. Y., Chauvaud, D., Jeanny, J. C., Chemtob, S., Behar-Cohen, F., and Sennlaub, F. (2007) CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration, J. Clin. Invest., 117, 2920–2928.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Luhmann, U. F., Robbie, S., Munro, P. M., Barker, S. E., Duran, Y., Luong, V., Fitzke, F. W., Bainbridge, J. W., Ali, R. R., and MacLaren, R. E. (2009) The drusen-like phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages, Invest. Ophthalmol. Vis. Sci., 50, 5934–5943.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Chan, C. C., Ross, R. J., Shen, D., Ding, X., Majumdar, Z., Bojanowski, C. M., Zhou, M., Salem, N., Jr., Bonner, R., and Tuo, J. (2008) Ccl2/Cx3cr1-deficient mice: an animal model for age-related macular degeneration, Ophthalm. Res., 40, 124–128.CrossRefGoogle Scholar
  72. 72.
    Pennesi, M. E., Neuringer, M., and Courtney, R. J. (2012) Animal models of age-related macular degeneration, Mol. Aspects Med., 33, 487–509.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Santos, A. M., Martin-Oliva, D., Ferrer-Martin, R. M., Tassi, M., Calvente, R., Sierra, A., Carrasco, M. C., Marin-Teva, J. L., Navascues, J., and Cuadros, M. A. (2010) Microglial response to light-induced photoprotector degeneration in the mouse retina, J. Comp. Neurol., 518, 477–492.CrossRefPubMedGoogle Scholar
  74. 74.
    Ma, W., Zhao, L., Fontainhas, A. M., Fariss, R. N., and Wong, W. T. (2009) Microglia in the mouse retina alter the structure and function of retinal pigmented epithelial cells: a potential cellular interaction relevant to AMD, PloS One, 4, e7945.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Ma, W., Zhao, L., and Wong, W. T. (2012) Microglia in the outer retina and their relevance to pathogenesis of agerelated macular degeneration, Adv. Exp. Med. Biol., 732, 37–42.CrossRefGoogle Scholar
  76. 76.
    Kozhevnikova, O. S., Korbolina, E. E., Ershov, N. I., and Kolosova, N. G. (2013) Rat retinal transcriptome: effects of aging and AMD-like retinopathy, Cell Cycle, 12, 1745–1761.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Perez, V. L., and Caspi, R. R. (2015) Immune mechanisms in inflammatory and degenerative eye disease, Trends Immunol., 36, 354–363.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Shaw, P. X., Stiles, T., Douglas, C., Ho, D., Fan, W., Du, H., and Xiao, X. (2016) Oxidative stress, innate immunity, and age-related macular degeneration, AIMS Mol. Sci., 3, 196–221.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Xu, H., and Chen, M. (2016) Targeting the complement system for the management of retinal inflammatory and degenerative diseases, Eur. J. Pharmacol., 787, 94–104.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • D. V. Telegina
    • 1
  • O. S. Kozhevnikova
    • 1
  • N. G. Kolosova
    • 1
    Email author
  1. 1.Institute of Cytology and GeneticsSiberian Branch of the Russian Academy of SciencesNovosibirskRussia

Personalised recommendations