Skip to main content
Log in

Role of the Redox System in Initiation of a Regenerative Response of Neural Eye Tissues in Vertebrates

  • REVIEWS
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The review examines the role of oxidative stress (OS) in the primary response of the neural eye tissue cells to damage and degenerative processes. The imbalance (homeostasis) of the redox system towards oxidative processes underlies the development of OS. OS can be used as a part of the protective mechanism initiating the processes of healing and regeneration of damaged tissues. Violation of redox homeostasis and OS development triggers an inflammatory response and immune response in the retina. The main reactions to stress (release of ATP, calcium ions, and reactive oxygen species (ROS) into the extracellular space, attraction of exogenous immune cells, activation of endogenous macro- and microglia, apoptosis of neurons) are universal and conservative in all vertebrates. However, with the similarity of some parts of cellular and molecular processes, there are evolutionary fixed functional differences in the regenerative response of retinal cells, and the final result in different vertebrate species is not equivalent. This determines the choice of regeneration strategies: activation of endogenous stem/progenitor cells and/or reprogramming of differentiated cells (retinal pigment epithelium, Müller glia). The detection of key signaling pathways, through which the effect of OS on regenerative responses is realized after damage and pathology of the neural tissues of the vertebral eye, will contribute to the choice of optimal strategies of the cell and/or gene therapy to activate the endogenic regenerative potential of retinal neural tissue in humans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Abdullayev, I., Kirkham, M., Bjorklund, A.K., et al., A reference transcriptome and inferred proteome for the salamander Notophthalmus viridescens,Exp. Cell Res., 2013, vol. 319, no. 8, pp. 1187–1197.

    Article  CAS  PubMed  Google Scholar 

  2. Ail, D. and Perron, M., Retinal degeneration and regeneration—lessons from fishes and amphibians, Curr. Pathobiol. Rep., 2017, vol. 5, no. 1, pp. 67–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Akhtar-Schafer, I., Wang, L., Krohne, T.U., et al., Modulation of three key innate immune pathways for the most common retinal degenerative diseases, EMBO Mol. Med., 2018, vol. 10, no. 10, pp. 1–27. e8259.

  4. Amano, S., Yamagishi, S., Inagaki, Y., et al., Pigment epithelium-derived factor inhibits oxidative stress-induced apoptosis and dysfunction of cultured retinal pericytes, Microvasc. Res., 2005, vol. 69, nos. 1–2, pp. 45–55.

    Article  CAS  PubMed  Google Scholar 

  5. Amram, B., Cohen-Tayar, Y., David, A., et al., The retinal pigmented epithelium - from basic developmental biology research to translational approaches, Int. J. Dev. Biol., 2017, vol. 61, nos. 3–4–5, pp. 225–234.

  6. Anders, H.J. and Schaefer, L., Beyond tissue injury-damage-associated molecular patterns, toll-like receptors, and inflammasomes also drive regeneration and fibrosis, J. Am. Soc. Nephrol., 2014, vol. 25, no. 7, pp. 1387–1400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Atienzar-Aroca, S., Flores-Bellver, M., Serrano-Heras, G., et al., Oxidative stress in retinal pigment epithelium cells increases exosome secretion and promotes angiogenesis in endothelial cells, J. Cell Mol. Med., 2016, vol. 20, no. 8, pp. 1457–1466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Aurora, A.B., Porrello, E.R., Tan, W., Mahmoud, A.I., Hill, J.A., Bassel-Duby, R., Sadek, H.A., and Olson, E.N., Macrophages are required for neonatal heart regeneration, J. Clin. Invest., 2014, vol. 124, no. 3, pp. 1382–1392.

  9. Babaeva, A.G., Reparative processes and immunity, Izv. Akad. Nauk, Ser. Biol., 1999, no. 6, pp. 261–269.

  10. Barbosa-Sabanero, K., Hoffmann, A., Judge, C., et al., Lens and retina regeneration: new perspectives from model organisms, Biochem. J., 2012, vol. 447, no. 3, pp. 321–334.

    Article  CAS  PubMed  Google Scholar 

  11. Beatty, S., Koh, H., Phil, M., et al., The role of oxidative stress in the pathogenesis of age-related macular degeneration, Surv. Ophthalmol., 2000, vol. 45, no. 2, pp. 115–134.

    Article  CAS  PubMed  Google Scholar 

  12. Belin, S., Nawabi, H., Wang, C., et al., Injury-induced decline of intrinsic regenerative ability revealed by quantitative proteomics, Neuron, 2015, vol. 86, no. 4, pp. 1000–1014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bely, A.E. and Nyberg, K.G., Evolution of animal regeneration: re-emergence of a field, Trends Ecol. Evol., 2010, vol. 25, no. 3, pp. 161–170.

    Article  PubMed  Google Scholar 

  14. Bennis, A., Gorgels, T.G., Ten Brink, J.B., et al., Comparison of mouse and human retinal pigment epithelium gene expression profiles: potential implications for age-related macular degeneration, PLoS One, 2015, vol. 10, no. 10. e0141597.

  15. Bhatia, B., Singhal, S., Jayaram, H., et al., Adult retinal stem cells revisited, Open Ophthalmol. J., 2010, vol. 4, pp. 30–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bi, Y.Y., Feng, D.F., and Pan, D.C., Stem/progenitor cells: a potential source of retina-specific cells for retinal repair, Neurosci. Res., 2009, vol. 65, no. 3, pp. 215–221.

    Article  CAS  PubMed  Google Scholar 

  17. Bindoli, A. and Rigobello, M.P., Principles in redox signaling: from chemistry to functional significance, Antioxid. Redox Signal., 2013, vol. 18, no. 13, pp. 1557–1593.

    Article  CAS  PubMed  Google Scholar 

  18. Blasiak, J., Petrovski, G., Vereb, Z., et al., Oxidative stress, hypoxia, and autophagy in the neovascular processes of age-related macular degeneration, Biomed. Res. Int., 2014, vol. 2014, p. 768026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Boda, E., Nato, G., and Buffo, A., Emerging pharmacological approaches to promote neurogenesis from endogenous glial cells, Biochem. Pharmacol., 2017, vol. 141, pp. 23–41.

    Article  CAS  PubMed  Google Scholar 

  20. Borquez, D.A., Urrutia, P.J., Wilson, C., et al., Dissecting the role of redox signaling in neuronal development, J. Neurochem., 2016, vol. 137, no. 4, pp. 506–517.

    Article  CAS  PubMed  Google Scholar 

  21. Bringmann, A., Iandiev, I., Pannicke, T., et al., Cellular signaling and factors involved in Müller cell gliosis: neuroprotective and detrimental effects, Prog. Retin. Eye Res., 2009, vol. 28, no. 6, pp. 423–451.

    Article  CAS  PubMed  Google Scholar 

  22. Campbell, L.J. and Hyde, D.R., Opportunities for CRISPR/ Cas9 gene editing in retinal regeneration research, Front. Cell Dev. Biol., 2017, vol. 5, art. 99, pp. 1–8.

  23. Casco-Robles, M.M., Islam, M.R., Inami, W., et al., Turning the fate of reprogramming cells from retinal disorder to regeneration by Pax6 in newts, Sci. Rep., 2016, vol. 6, p. 33761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chen, H.Y., Kaya, K.D., Dong, L., et al., Three-dimensional retinal organoids from mouse pluripotent stem cells mimic in vivo development with enhanced stratification and rod photoreceptor differentiation, Mol. Vis., 2016, vol. 22, pp. 1077–1094.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Cherenkevich, S.N., Martinovich, G.G., Martinovich, I.V., et al., Redox homeostasis of biological systems: theory and practice, Zh. Gr. Gos. Med. Univ., 2009, no. 2, pp. 9–11.

  26. Chiba, C., The retinal pigment epithelium: an important player of retinal disorders and regeneration, Exp. Eye Res., 2014, vol. 123, pp. 107–114.

    Article  CAS  PubMed  Google Scholar 

  27. Chiba, C. and Mitashov, V.I., Cellular and molecular events in the adult newt retinal regeneration, in The Strategies for Retinal Tissue Repair and Regeneration in Vertebrates: From Fish to Human, Chiba, C., Ed., Kerala, India: Res. Signpost, 2007, pp. 15–33.

    Google Scholar 

  28. Chiba, C., Hoshino, A., Nakamura, K., et al., Visual cycle protein RPE65 persists in new retinal cells during retinal regeneration of adult newt, J. Comp. Neurol., 2006, vol. 495, no. 4, pp. 391–407.

    Article  CAS  PubMed  Google Scholar 

  29. Cho, Y., Shin, J.E., Ewan, E.E., et al., Activating injury-responsive genes with hypoxia enhances axon regeneration through neuronal HIF-1α, Neuron, 2015, vol. 88, no. 4, pp. 720–734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chung, J.W., Spot the difference: solving the puzzle of hidden pictures in the lizard genome for identification of regeneration factors, BMB Rep., 2016, vol. 49, no. 5, pp. 249–254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Conedera, F.M., Pousa, A.M.Q., Mercader, N., et al., Retinal microglia signaling affects Müller cell behavior in the zebrafish following laser injury induction, Glia, 2019, vol. 67, no. 6, pp. 1150–1166.

    Article  PubMed  Google Scholar 

  32. Cordeiro, J.V. and Jacinto, A., The role of transcription-independent damage signals in the initiation of epithelial wound healing, Nat. Rev. Mol. Cell Biol., 2013, vol. 14, no. 4, pp. 249–262.

    Article  CAS  PubMed  Google Scholar 

  33. Cuenca, N., Fernandez-Sanchez, L., Campello, L., et al., Cellular responses following retinal injuries and therapeutic approaches for neurodegenerative diseases, Prog. Retin. Eye Res., 2014, vol. 43, pp. 17–75.

    Article  CAS  PubMed  Google Scholar 

  34. Cunha-Vaz, J., Bernardes, R., and Lobo, C., Blood-retinal barrier, Eur. J. Ophthalmol., 2011, vol. 21, suppl. 6, pp. 3–9.

    Article  Google Scholar 

  35. Cvekl, A. and Mitton, K.P., Epigenetic regulatory mechanisms in vertebrate eye development and disease, Heredity (Edinb.), 2010, vol. 105, no. 1, pp. 135–151.

    Article  CAS  Google Scholar 

  36. Das, A.V., Mallya, K.B., Zhao, X., et al., Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling, Dev. Biol., 2006, vol. 299, no. 1, pp. 283–302.

    Article  CAS  PubMed  Google Scholar 

  37. Delyfer, M.N., Raffelsberger, W., and Mercier, D., Transcriptomic analysis of human retinal detachment reveals both inflammatory response and photoreceptor death, PLoS One, 2011, vol. 6, no. 12. e28791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Diaz-Coranguez, M., Ramos, C., and Antonetti, D.A., The inner blood-retinal barrier: cellular basis and development, Vision Res., 2017, vol. 139, pp. 123–137.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Dieudonne, S.C., La Heij, E.C., Diederen, R., et al., High TGF-beta2 levels during primary retinal detachment may protect against proliferative vitreoretinopathy, Invest. Ophthalmol. Vis. Sci., 2004, vol. 45, no. 11, pp. 4113–4118.

    Article  PubMed  Google Scholar 

  40. DiStefano, T., Chen, H.Y., Panebianco, C., et al., Accelerated and improved differentiation of retinal organoids from pluripotent stem cells in rotating-wall vessel bioreactors, Stem Cell Reports, 2018, vol. 10, no. 1, pp. 300–313.

    Article  CAS  PubMed  Google Scholar 

  41. Dvoriantchikova, G. and Ivanov, D., Tumor necrosis factor-alpha mediates activation of NF-κB and JNK signaling cascades in retinal ganglion cells and astrocytes in opposite ways, Eur. J. Neurosci., 2014, vol. 40, no. 8, pp. 3171–3178.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Dvoriantchikova, G., Seemungal, R.J., and Ivanov, D., The epigenetic basis for the impaired ability of adult murine retinal pigment epithelium cells to regenerate retinal tissue, Sci. Rep., 2019, vol. 9, no. 1, pp. 1–13.

    Article  CAS  Google Scholar 

  43. Elewa, A., Wang, H., and Talavera-Lopez, C., Reading and editing the Pleurodeles waltl genome reveals novel features of tetrapod regeneration, Nat. Commun., 2017, vol. 8, no. 1, pp. 1–9.

    Article  CAS  Google Scholar 

  44. Emanuele, S., D’Anneo, A., Calvaruso, G., et al., The double-edged sword profile of redox signaling: oxidative events as molecular switches in the balance between cell physiology and cancer, Chem. Res. Toxicol., 2018, vol. 31, no. 4, pp. 201–210.

    Article  CAS  PubMed  Google Scholar 

  45. Erler, P. and Monaghan, J.R., The link between injury-induced stress and regenerative phenomena: a cellular and genetic synopsis, Biochim. Biophys. Acta, 2015, vol. 1849, no. 4, pp. 454–461.

    Article  CAS  PubMed  Google Scholar 

  46. Ferretti, P., Is there a relationship between adult neurogenesis and neuron generation following injury across evolution?, Eur. J. Neurosci., 2011, vol. 34, no. 6, pp. 951–962.

    Article  PubMed  Google Scholar 

  47. Fischer, R. and Maier, O., Interrelation of oxidative stress and inflammation in neurodegenerative disease: role of TNF, Oxid. Med. Cell. Longev., 2015, vol. 2015, article ID 610813, pp. 1–18.

  48. Fischer, A.J. and Reh, T.A., Exogenous growth factors stimulate the regeneration of ganglion cells in the chicken retina, Dev. Biol., 2002, vol. 251, no. 2, pp. 367–379.

    Article  CAS  PubMed  Google Scholar 

  49. Fisher, S.K., Lewis, G.P., Linberg, K.A., et al., Cellular remodeling in mammalian retina induced by retinal detachment, in Webvision: The Organization of the Retina and Visual System [Internet], Kolb, H., Fernandez, E., and Nelson, R., Eds., University of Utah Health Sciences Center, Salt Lake City, UT, USA, 2007, pp. 1–51.

    Google Scholar 

  50. Fuhrmann, S., Eye morphogenesis and patterning of the optic vesicle, Curr. Top. Dev. Biol., 2010, vol. 93, pp. 61–84.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Fukui, M. and Zhu, B.T., Mitochondrial superoxide dismutase SOD2, but not cytosolic SOD1, plays a critical role in protection against glutamate-induced oxidative stress and cell death in HT22 neuronal cells, Free Radic. Biol. Med., 2010, vol. 48, no. 6, pp. 821–830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Galliot, B. and Chera, S., The hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration, Trends Cell Biol., 2010, vol. 20, no. 9, pp. 514–523.

    Article  CAS  PubMed  Google Scholar 

  53. Galliot, B. and Ghila, L., Cell plasticity in homeostasis and regeneration, Mol. Reprod. Dev., 2010, vol. 77, no. 10, pp. 837–855.

    Article  CAS  PubMed  Google Scholar 

  54. Galliot, B., Crescenzi, M., Jacinto, A., et al., Trends in tissue repair and regeneration, Development, 2017, vol. 144, no. 3, pp. 357–364.

    Article  CAS  PubMed  Google Scholar 

  55. Galluzzi, L., Bravo-San Pedro, J.M., Kepp, O., et al., Regulated cell death and adaptive stress responses, Cell. Mol. Life Sci., 2016, vol. 73, nos. 11–12, pp. 2405–2410.

    Article  CAS  PubMed  Google Scholar 

  56. Gasparini, S.J., Llonch, S., Borsch, O., et al., Transplantation of photoreceptors into the degenerative retina: current state and future perspectives, Prog. Retin. Eye Res., 2019, vol. 69, pp. 1–37.

    Article  CAS  PubMed  Google Scholar 

  57. Geller, S.F., Lewis, G.P., and Fisher, S.K., Fgfr1, signaling, and ap-1 expression after retinal detachment: reactive Müller and RPE cells, Invest. Ophthalmol. Vis. Sci., 2001, vol. 42, pp. 1363–1369.

    CAS  PubMed  Google Scholar 

  58. Genini, S., Beltran, W.A., Stein, V.M., et al., Isolation and ex vivo characterization of the immunophenotype and function of microglia/macrophage populations in normal dog retina, Adv. Exp. Med. Biol., 2014, vol. 801, pp. 339–345.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Grigoryan, E.N., Shared triggering mechanisms of retinal regeneration in lower vertebrates and retinal rescue in higher ones, in Tissue Regeneration—From Basic Biology to Clinical Application, Davies, J., Ed., Croatia: In Tech, 2012, pp. 145–164.

  60. Grigoryan, E.N. and Markitantova, Y.V., Cellular and molecular preconditions for retinal pigment epithelium (RPE) natural reprogramming during retinal regeneration in Urodela, Biomedicines, 2016, vol. 4, no. 4, pii: E28, pp. 1–18.

  61. Hameed, L.S., Berg, D.A., Belnoue, L., et al., Environmental changes in oxygen tension reveal ROS-dependent neurogenesis and regeneration in the adult newt brain, Elife, 2015, vol. 20, no. 4, pii: e08422, pp. 1–16.

  62. Hamon, A., Roger, J.E., Yang, X.J., et al., Müller glial cell-dependent regeneration of the neural retina: an overview across vertebrate model systems, Dev. Dyn., 2016, vol. 245, no. 7, pp. 727–738.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Haynes, T., Luz-Madrigal, A., Reis, E.S., et al., Complement anaphylatoxin C3a is a potent inducer of embryonic chick retina regeneration, Nat. Commun., 2013, vol. 4, p. 2312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hoon, M., Okawa, H., Della Santina, L., et al., Functional architecture of the retina: development and disease, Prog. Retin. Eye Res., 2014, vol. 42, pp. 44–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. de Hoz, R., Rojas, B., Ramírez, A.I., et al., Retinal macroglial responses in health and disease, Biomed. Res. Int., 2016, vol. 2016, article ID 2954721, pp. 1–13.

  66. Hunter, J.J., Morgan, J.I., Merigan, W.H., et al., The susceptibility of the retina to photochemical damage from visible light, Prog. Retin. Eye Res., 2012, vol. 31, no. 1, pp. 28–42.

    Article  PubMed  Google Scholar 

  67. Inami, W., Islam, M.R., Nakamura, K., et al., Expression of two classes of pax6 transcripts in reprogramming retinal pigment epithelium cells of the adult newt, Zoolog. Sci., 2016, vol. 33, no. 1, pp. 21–30.

    Article  CAS  PubMed  Google Scholar 

  68. Iqbal, J., Zhang, K., Jin, N., et al., Alzheimer’s disease is responsible for progressive age-dependent differential expression of various protein cascades in retina of mice, ACS Chem. Neurosci., 2019. https://doi.org/10.1021/acschemneuro.8b00710

  69. Isenmann, S., Kretz, A., and Cellerino, A., Molecular determinants of retinal ganglion cell development, survival, and regeneration, Prog. Retin. Eye Res., 2003, vol. 22, no. 4, pp. 483–543.

    Article  CAS  PubMed  Google Scholar 

  70. Islam, M.R., Nakamura, K., Casco-Robles, M.M., et al., The newt reprograms mature RPE cells into a unique multipotent state for retinal regeneration, Sci. Rep., 2014, vol. 4, pp. 1–8.

    Google Scholar 

  71. Jacobs, A.T. and Marnett, L.J., Systems analysis of protein modification and cellular responses induced by electrophile stress, Acc. Chem. Res., 2010, vol. 43, no. 5, pp. 673–683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Jarrett, S.G. and Boulton, M.E., Antioxidant up-regulation and increased nuclear DNA protection play key roles in adaptation to oxidative stress in epithelial cells, Free Radic. Biol. Med., 2005, vol. 38, no. 10, pp. 1382–1391.

    Article  CAS  PubMed  Google Scholar 

  73. Jorstad, N.L., Wilken, M.S., Grimes, W.N., et al., Stimulation of functional neuronal regeneration from Müller glia in adult mice, Nature, 2017, vol. 548, no. 7665, pp. 103–107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kaneko, Y., Matsumoto, G., Hanyu, Y., et al., The occurrence of apoptosis during retinal regeneration in adult newts, Brain Res. Dev. Brain Res., 1999, vol. 117, no. 2, pp. 225–228.

    Article  CAS  PubMed  Google Scholar 

  75. Kang, M.K., Lee, E.J., Kim, Y.H., et al., Chrysin ameliorates malfunction of retinoid visual cycle through blocking activation of AGE-RAGE-ER stress in glucose-stimulated retinal pigment epithelial cells and diabetic eyes, Nutrients, 2018, vol. 10, no. 8. pii: E1046.

    Article  CAS  PubMed  Google Scholar 

  76. Katsman, D., Stackpole, E.J., Domin, D.R., et al., Embryonic stem cell-derived microvesicles induce gene expression changes in Müller cells of the retina, PLoS One, 2012, vol. 7, no. 11. e50417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Keeling, E., Lotery, A.J., Tumbarello, D.A., et al., Impaired cargo clearance in the retinal pigment epithelium (RPE) underlies irreversible blinding diseases, Cells, 2018, vol. 7, no. 2. pii: E16.

    Article  CAS  PubMed  Google Scholar 

  78. Kimelberg, H.K., Functions of mature mammalian astrocytes: a current view, Neuroscientist, 2010, vol. 16, no. 1, pp. 79–106.

    Article  CAS  PubMed  Google Scholar 

  79. Kirchhof, B. and Sorgente, N., Pathogenesis of proliferative vitreoretinopathy. Modulation of retinal pigment epithelial cell functions by vitreous and macrophages, Dev. Ophthalmol., 1989, vol. 16, pp. 1–53.

    Article  CAS  PubMed  Google Scholar 

  80. Kolb, H., Outer plexiform layer, in Webvision: The Organization of the Retina and Visual System [Internet], Kolb, H., Fernandez, E., and Nelson, R., Eds., University of Utah Health Sciences Center, Salt Lake City, UT, USA, 2007a.

    Google Scholar 

  81. Kolb, H., Inner plexiform layer, in Webvision: The Organization of the Retina and Visual System [Internet], Kolb, H., Fernandez, E., and Nelson, R., Eds., University of Utah Health Sciences Center, Salt Lake City, UT, USA, 2007b.

    Google Scholar 

  82. Kolb, H., Simple anatomy of the retina, in Webvision: The Organization of the Retina and Visual System [Internet], Kolb, H., Fernandez, E., and Nelson, R., Eds., University of Utah Health Sciences Center, Salt Lake City, UT, USA, 2012.

    Google Scholar 

  83. Kortuem, K., Geiger, L.K., and Levin, L.A., Differential susceptibility of retinal ganglion cells to reactive oxygen species, Invest. Ophthalmol. Vis. Sci., 2000, vol. 41, no. 10, pp. 3176–3182.

    CAS  PubMed  Google Scholar 

  84. Kostas, M., Lampart, A., Bober, J., et al., Translocation of exogenous FGF1 and FGF2 protects the cell against apoptosis independently of receptor activation, J. Mol. Biol., 2018, vol. 430, no. 21, pp. 4087–4101.

    Article  CAS  PubMed  Google Scholar 

  85. Kozakowska, M., Pietraszek-Gremplewicz, K., Jozkowicz, A., et al., The role of oxidative stress in skeletal muscle injury and regeneration: focus on antioxidant enzymes, J. Muscle Res. Cell Motil., 2015, vol. 36, no. 6, pp. 377–393.

    Article  CAS  PubMed  Google Scholar 

  86. Kumaramanickavel, G., Age-related macular degeneration: genetics and biology, Asia Pac. J. Ophthalmol. (Phila), 2016, vol. 5, no. 4, pp. 229–235.

    Article  CAS  Google Scholar 

  87. Lamb, T.D., Evolution of phototransduction, vertebrate photoreceptors and retina, Prog. Retin. Eye Res., 2013, vol. 36, pp. 52–119.

    Article  CAS  PubMed  Google Scholar 

  88. Langhe, R., Chesneau, A., Colozza, G., et al., Müller glial cell reactivation in Xenopus models of retinal degeneration, Glia, 2017, vol. 65, no. 8, pp. 1333–1349.

    Article  PubMed  Google Scholar 

  89. Leaver, S.G., Cui, Q., Plant, G.W., et al., AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells, Gene Ther., 2006, vol. 13, no. 18, pp. 1328–1341.

    Article  CAS  PubMed  Google Scholar 

  90. Lenkowski, J.R. and Raymond, P.A., Müller glia: stem cells for generation and regeneration of retinal neurons in teleost fish, Prog. Retin. Eye Res., 2014, vol. 40, pp. 94–123.

    Article  PubMed  Google Scholar 

  91. Leveillard, T. and Sahel, J.A., Metabolic and redox signaling in the retina, Cell Mol. Life Sci., 2017, vol. 74, no. 20, pp. 3649–3665.

    Article  CAS  PubMed  Google Scholar 

  92. Li, F., Huang, Q., Chen, J., et al., Apoptotic cells activate the “phoenix rising” pathway to promote wound healing and tissue regeneration, Sci. Signal., 2010, vol. 3, no. 110. ra13, pp. 1–20.

  93. Llonch, S., Carido, M., and Ader, M., Organoid technology for retinal repair, Dev. Biol., 2018, vol. 433, no. 2, pp. 132–143.

    Article  CAS  PubMed  Google Scholar 

  94. Logan, A., Ahmed, Z., Baird, A., et al., Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury, Brain, 2006, vol. 129, pt 2, pp. 490–502.

    Article  PubMed  Google Scholar 

  95. Love, N.R., Chen, Y., Ishibashi, S., et al., Amputation-induced reactive oxygen species are required for successful Xenopus tadpole tail regeneration, Nat. Cell Biol., 2013, vol. 15, no. 2, pp. 222–228.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Lu, Q., Cui, Q., Yip, H.K., et al., c-Jun expression in surviving and regenerating retinal ganglion cells: effects of intravitreal neurotrophic supply, Invest. Ophthalmol. Vis. Sci., 2003, vol. 44, no. 12, pp. 5342–5348.

    Article  PubMed  Google Scholar 

  97. Lushchak, V.I., Adaptive response to oxidative stress: bacteria, fungi, plants and animals, Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 2011, vol. 153, no. 2, pp. 175–190.

    Article  CAS  PubMed  Google Scholar 

  98. Ma, W., Zhang, Y., Gao, C., et al., Monocyte infiltration and proliferation reestablish myeloid cell homeostasis in the mouse retina following retinal pigment epithelial cell injury, Sci. Rep., 2017, vol. 7, no. 1, 8433, pp. 1–18.

    Article  CAS  Google Scholar 

  99. Markitantova, Yu.V., Avdonin, P.P., and Grigoryan, E.N., Specific activity of fibroblast growth factor 2 and nucleostemin in forming vertebrate retina, in Nauchnaya konferentsiya s mezhdunarodnym uchastiem “Aktual’nye voprosy morfogeneza v norme i patologii”, 6–7 aprelya 2016, Moskva. Sbornik nauchnykh trudov” (Sci. Conf. with Int. Particip. “Topical Issues of Morphogenesis in Health and Disease,” April 6–7, 2016, Moscow. Collected Scientific Papers), Moscow: Gruppa MDV, 2016, pp. 107–108.

  100. Masutomi, K., Chen, C., Nakatani, K., et al., All-trans retinal mediates light-induced oxidation in single living rod photoreceptors, Photochem. Photobiol., 2012, vol. 88, no. 6, pp. 1356–1361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Mazzolini, M., Facchetti, G., Andolfi, L., et al., The phototransduction machinery in the rod outer segment has a strong efficacy gradient, Proc. Natl. Acad. Sci. U. S. A., 2015, vol. 112, no. 20, pp. E2715–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Meda, F., Rampon, C., Dupont, E., et al., Nerves, H2O2 and Shh: three players in the game of regeneration, Semin. Cell Dev. Biol., 2018, vol. 80, pp. 65–73.

    Article  CAS  PubMed  Google Scholar 

  103. Mishra, S., Maurya, Sh.K., Srivastava, K., Shukla, S., and Mishra, R., Pax6 influences expression patterns of genes involved in neurodegeneration, Ann. Neurosci., 2015, vol. 22, no. 4, pp. 226–231.https://doi.org/10.5214/ans.0972.7531.220407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Mitashov, V.I., Mechanisms of retina regeneration in urodeles, Int. J. Dev. Biol., 1996, vol. 40, no. 4, pp. 833–844.

    CAS  PubMed  Google Scholar 

  105. Mitashov, V.I., Retinal regeneration in amphibians, Int. J. Dev. Biol., 1997, vol. 41, no. 6, pp. 893–905.

    CAS  PubMed  Google Scholar 

  106. Mitchell, C.H., Lu, W., Hu, H., et al., The P2X(7) receptor in retinal ganglion cells: a neuronal model of pressure-induced damage and protection by a shifting purinergic balance, Purinergic Signal., 2008, vol. 4, no. 4, pp. 313–321.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Mitra, S., Sharma, P., Kaur, S., et al., Dual regulation of lin28a by Myc is necessary during zebrafish retina regeneration, J. Cell Biol., 2019, vol. 218, no. 2, pp. 489–507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Moldogazieva, N.T., Mokhosoev, I.M., Feldman, N.B., et al., ROS and RNS signalling: adaptive redox switches through oxidative/nitrosative protein modifications, Free Radic. Res., 2018, vol. 52, no. 5, pp. 507–543.

    Article  CAS  PubMed  Google Scholar 

  109. Murawala, P., Tanaka, E.M., and Currie, J.D., Regeneration: the ultimate example of wound healing, Semin. Cell Dev. Biol., 2012, vol. 23, no. 9, pp. 954–962.

    Article  CAS  PubMed  Google Scholar 

  110. Nabeshima, A., Nishibayashi, C., Ueda, Y., et al., Loss of cell-extracellular matrix interaction triggers retinal regeneration accompanied by Rax and Pax6 activation, Genesis, 2013, vol. 51, no. 6, pp. 410–419.

    Article  CAS  PubMed  Google Scholar 

  111. Nagashima, M., Fujikawa, C., Mawatari, K., et al., HSP70, the earliest-induced gene in the zebrafish retina during optic nerve regeneration: its role in cell survival, Neurochem. Int., 2011, vol. 58, no. 8, pp. 888–895.

    Article  CAS  PubMed  Google Scholar 

  112. Nakamura, K. and Chiba, C., Evidence for Notch signaling involvement in retinal regeneration of adult newt, Brain Res., 2007, vol. 1136, no. 1, pp. 28–42.

    Article  CAS  PubMed  Google Scholar 

  113. Nakamura, K., Islam, M.R., Takayanagi, M., et al., A transcriptome for the study of early processes of retinal regeneration in the adult newt, Cynops pyrrhogaster, PLoS One, 2014, vol. 9, no. 10, e109831, pp. 1–12.

  114. Nakanishi, T., Shimazawa, M., Sugitani, S., et al., Role of endoplasmic reticulum stress in light-induced photoreceptor degeneration in mice, J. Neurochem., 2013, vol. 125, no. 1, pp. 111–124.

    Article  CAS  PubMed  Google Scholar 

  115. Nakanishi-Ueda, T., Majima, H.J., Watanabe, K., et al., Blue LED light exposure develops intracellular reactive oxygen species, lipid peroxidation, and subsequent cellular injuries in cultured bovine retinal pigment epithelial cells, Free Radic. Res., 2013, vol. 47, no. 10, pp. 774–780.

    Article  CAS  PubMed  Google Scholar 

  116. Nakazawa, T., Matsubara, A., Noda, K., et al., Characterization of cytokine responses to retinal detachment in rats, Mol. Vis., 2006, vol. 12, pp. 867–878.

    CAS  PubMed  Google Scholar 

  117. Neves, J., Zhu, J., Sousa-Victor, P., et al., Immune modulation by MANF promotes tissue repair and regenerative success in the retina, Science, 2016, vol. 353, no. 6294. aaf3646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Newman, E.A., Glial cell regulation of neuronal activity and blood flow in the retina by release of gliotransmitters, Philos. Trans. R. Soc. Lond. Ser. Biol., 2015, vol. 370, no. 1672.

  119. Noro, T., Namekata, K., Kimura, A., et al., Spermidine promotes retinal ganglion cell survival and optic nerve regeneration in adult mice following optic nerve injury, Cell Death Dis., 2015, vol. 6. e1720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Nowoshilow, S., Schloissnig, S., Fei, J.F., et al., The axolotl genome and the evolution of key tissue formation regulators, Nature, 2018, vol. 554, no. 7690, pp. 50–55.

    Article  CAS  PubMed  Google Scholar 

  121. Osakada, F., Ooto, S., Akagi, T., et al., Wnt signaling promotes regeneration in the retina of adult mammals, J. Neurosci., 2007, vol. 27, no. 15, pp. 4210–4219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Perez-Torres, I., Guarner-Lans, V., and Rubio-Ruiz, M.E., Reductive stress in inflammation-associated diseases and the pro-oxidant effect of antioxidant agents, Int. J. Mol. Sci., 2017, vol. 18, no. 10. pii: E2098, pp. 1–26.

  123. Powell, C., Grant, A.R., Cornblath, E., et al., Analysis of DNA methylation reveals a partial reprogramming of the Müller glia genome during retina regeneration, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 49, pp. 19814–19819.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Rao, M.B., Didiano, D., and Patton, J.G., Neurotransmitter-regulated regeneration in the zebrafish retina, Stem Cell Rep., 2017, vol. 8, no. 4, pp. 831–842.

    Article  CAS  Google Scholar 

  125. Ray, P.D., Huang, B.W., and Tsuji, Y., Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling, Cell Signal., 2012, vol. 24, no. 5, pp. 981–990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Reczek, C.R. and Chandel, N.S., ROS-dependent signal transduction, Curr. Opin. Cell Biol., 2015, vol. 33, pp. 8–13.

    Article  CAS  PubMed  Google Scholar 

  127. Reichenbach, A. and Bringmann, A., New functions of Müller cells, Glia, 2013, vol. 61, no. 5, pp. 651–678.

    Article  PubMed  Google Scholar 

  128. Reichenbach, A. and Bringmann, A., Role of purines in Müller glia, J. Ocul. Pharmacol. Ther., 2016, vol. 32, no. 8, pp. 518–533.

    Article  CAS  PubMed  Google Scholar 

  129. Roehlecke, C., Schumann, U., Ader, M., et al., Stress reaction in outer segments of photoreceptors after blue light irradiation, PLoS One, 2013, vol. 8, no. 9, e71570, pp. 1–12.

  130. Roy, S. and Levesque, M., Limb regeneration in axolotl: is it superhealing?, Sci. World J., 2006, vol. 6, suppl. 1, pp. 12–25.

    Article  Google Scholar 

  131. Salero, E., Blenkinsop, T.A., Corneo, B., et al., Adult human RPE can be activated into a multipotent stem cell that produces mesenchymal derivatives, Cell Stem Cell, 2012, vol. 10, no. 1, pp. 88–95.

    Article  CAS  PubMed  Google Scholar 

  132. Sanes, J.R. and Masland, R.H., The types of retinal ganglion cells: current status and implications for neuronal classification, Annu. Rev. Neurosci., 2015, vol. 38, pp. 221–246.

    Article  CAS  PubMed  Google Scholar 

  133. Sato, K., Saigusa, D., Saito, R., et al., Metabolomic changes in the mouse retina after optic nerve injury, Sci. Rep., 2018, vol. 8, no. 1, p. 11930.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Schlingemann, R.O., Role of growth factors and the wound healing response in age-related macular degeneration, Graefes Arch. Clin. Exp. Ophthalmol., 2004, vol. 242, no. 1, pp. 91–101.

    Article  CAS  PubMed  Google Scholar 

  135. Seagle, B.L., Rezai, K.A., Gasyna, E.M., et al., Time-resolved detection of melanin free radicals quenching reactive oxygen species, J. Am. Chem. Soc., 2005, vol. 127, no. 32, pp. 11220–11221.

    Article  CAS  PubMed  Google Scholar 

  136. Selvam, S., Kumar, T., and Fruttiger, M., Retinal vasculature development in health and disease, Prog. Retin. Eye Res., 2018, vol. 63, pp. 1–19.

    Article  CAS  PubMed  Google Scholar 

  137. Sharma, T.P., McDowell, C.M., Liu, Y., et al., Optic nerve crush induces spatial and temporal gene expression patterns in retina and optic nerve of BALB/cJ mice, Mol. Neurodegener., 2014, vol. 9, no. 14, pp. 1–19.

    Article  CAS  Google Scholar 

  138. Sies, H., Berndt, C., and Jones, D.P., Oxidative stress, Annu. Rev. Biochem., 2017, vol. 86, pp. 715–748.

    Article  CAS  PubMed  Google Scholar 

  139. Sifuentes, C.J., Kim, J.W., Swaroop, A., et al., Rapid, dynamic activation of Müller glial stem cell responses in zebrafish, Invest. Ophthalmol. Vis. Sci., 2016, vol. 57, no. 13, pp. 5148–5160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Simo, R. and Hernandez, C., European consortium for the early treatment of diabetic retinopathy (EUROCONDOR) neurodegeneration in the diabetic eye: new insights and therapeutic perspectives, Trends Endocrinol. Metabol., 2014, vol. 25, no. 1, pp. 23–33.

    Article  CAS  Google Scholar 

  141. Simon, M.V., Agnolazza, D.L., German, O.L., et al., Synthesis of docosahexaenoic acid from eicosapentaenoic acid in retina neurons protects photoreceptors from oxidative stress, J. Neurochem., 2016, vol. 136, no. 5, pp. 931–946.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Singh, R., Cuzzani, O., Binette, F., et al., Pluripotent stem cells for retinal tissue engineering: current status and future prospects, Stem Cell Rev., 2018, vol. 14, no. 4, pp. 463–483.

    Article  PubMed Central  Google Scholar 

  143. Slack, J.M., Beck, C.W., Gargioli, C., et al., Cellular and molecular mechanisms of regeneration in Xenopus, Philos. Trans. R Soc. Lond.,Ser. Biol., 2004, vol. 359, no. 1445, pp. 745–751.

    CAS  Google Scholar 

  144. Solberg, R., Escobar, J., Arduini, A., et al., Metabolomic analysis of the effect of postnatal hypoxia on the retina in a newly born piglet model, PLoS One, 2013, vol. 8, no. 6. e66540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Sousounis, K., Looso, M., Maki, N., et al., Transcriptome analysis of newt lens regeneration reveals distinct gradients in gene expression patterns, PLoS One, 2013, no. 4, p. 8. e61445.

  146. Sousounis, K., Bhavsar, R., Looso, M., et al., Molecular signatures that correlate with induction of lens regeneration in newts: lessons from proteomic analysis, Hum. Genomics, 2014, vol. 8, 22, pp. 1–16.

    Article  CAS  Google Scholar 

  147. Stevenson, L., Matesanz, N., Colhoun, L., et al., Reduced nitro-oxidative stress and neural cell death suggests a protective role for microglial cells in TNFalpha–/– mice in ischemic retinopathy, Invest. Ophthalmol. Vis. Sci., 2010, vol. 51, no. 6, pp. 3291–3299.

    Article  PubMed  PubMed Central  Google Scholar 

  148. Strauss, O., The retinal pigment epithelium in visual function, Physiol. Rev., 2005, vol. 85, no. 3, pp. 845–881.

    Article  CAS  PubMed  Google Scholar 

  149. Subirada, P.V., Paz, M.C., Ridano, M.E., et al., A journey into the retina: Müller glia commanding survival and death, Eur. J. Neurosci., 2018, vol. 47, no. 12, pp. 1429–1443.

    Article  PubMed  Google Scholar 

  150. Sun, M., Finnemann, S.C., Febbraio, M., et al., Light-induced oxidation of photoreceptor outer segment phospholipids generates ligands for CD36-mediated phagocytosis by retinal pigment epithelium: a potential mechanism for modulating outer segment phagocytosis under oxidant stress conditions, J. Biol. Chem., 2006, vol. 281, no. 7, pp. 4222–4230.

    Article  CAS  PubMed  Google Scholar 

  151. Suzuki, N. and Mittler, R., Reactive oxygen species-dependent wound responses in animals and plants, Free Radic. Biol. Med., 2012, vol. 53, no. 12, pp. 2269–2276.

    Article  CAS  PubMed  Google Scholar 

  152. Tate, D.J., Jr., Miceli, M.V., and Newsome, D.A., Phagocytosis and H2O2 induce catalase and metallothionein gene expression in human retinal pigment epithelial cells, Invest. Ophthalmol. Vis. Sci., 1995, vol. 36, no. 7, pp. 1271–1279.

    PubMed  Google Scholar 

  153. Todd, L., Suarez, L., Quinn, C., et al., Retinoic acid-signaling regulates the proliferative and neurogenic capacity of Müller glia-derived progenitor cells in the avian retina, Stem Cells, 2018, vol. 36, no. 3, pp. 392–405.

    Article  CAS  PubMed  Google Scholar 

  154. Tokarz, P., Kaarniranta, K., and Blasiak, J., Role of antioxidant enzymes and small molecular weight antioxidants in the pathogenesis of age-related macular degeneration (AMD), Biogerontology, 2013, vol. 14, no. 5, pp. 461–482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Tonges, L., Ostendorf, T., Lamballe, F., et al., Hepatocyte growth factor protects retinal ganglion cells by increasing neuronal survival and axonal regeneration in vitro and in vivo, J. Neurochem., 2011, vol. 117, no. 5, pp. 892–903.

    Article  CAS  PubMed  Google Scholar 

  156. Trachootham, D., Lu, W., Ogasawara, M.A., et al., Redox regulation of cell survival, Antioxid. Redox Signal., 2008, vol. 10, no. 8, pp. 1343–1374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Trost, A., Bruckner, D., Rivera, F.J., et al., Pericytes in the retina, Adv. Exp. Med. Biol., 2019, vol. 1122, pp. 1–26.

    Article  CAS  PubMed  Google Scholar 

  158. Tsukamoto, Y., Morphological survey from neurons to circuits of the mouse retina, Methods Mol. Biol., 2018, vol. 1753, pp. 3–25.

    Article  CAS  PubMed  Google Scholar 

  159. Ueta, T., Inoue, T., Furukawa, T., et al., Glutathione peroxidase 4 is required for maturation of photoreceptor cells, J. Biol. Chem., 2012, vol. 287, no. 10, pp. 7675–7682.

    Article  CAS  PubMed  Google Scholar 

  160. Usui, S., Oveson, B.C., Iwase, T., et al., Overexpression of sod in retina: need for increase in H2O2-detoxifying enzyme in same cellular compartment, Free Radic. Biol. Med., 2011, vol. 51, no. 7, pp. 1347–1354.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Vigneswara, V., Esmaeili, M., Deer, L., et al., Eye drop delivery of pigment epithelium-derived factor-34 promotes retinal ganglion cell neuroprotection and axon regeneration, Mol. Cell. Neurosci., 2015, vol. 68, pp. 212–221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. van der Vliet, A. and Janssen-Heininger, Y.M., Hydrogen peroxide as a damage signal in tissue injury and inflammation: murderer, mediator, or messenger?, J. Cell. Biochem., 2014, vol. 115, no. 3, pp. 427–435.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Vriz, S., Reiter, S., and Galliot, B., Cell death: a program to regenerate, Curr. Top. Dev. Biol., 2014, vol. 108, pp. 121–151.

    Article  CAS  PubMed  Google Scholar 

  164. Wan, J. and Goldman, D., Retina regeneration in zebrafish, Curr. Opin. Genet. Dev., 2016, vol. 40, pp. 41–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Wan, J., Ramachandran, R., and Goldman, D., HB-EGF is necessary and sufficient for Müller glia dedifferentiation and retina regeneration, Dev. Cell, 2012, vol. 22, no. 2, pp. 334–347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Wang, Z., Dillon, J., and Gaillard, E.R., Antioxidant properties of melanin in retinal pigment epithelial cells, Photochem. Photobiol., 2006, vol. 82, no. 2, pp. 474–479.

    Article  CAS  PubMed  Google Scholar 

  167. Wang, S., Chu, C.H., Stewart, T., et al., α-Synuclein, a chemoattractant, directs microglial migration via H2O2-dependent Lyn phosphorylation, Proc. Natl. Acad. Sci. U. S. A., 2015, vol. 112, no. 15, pp. E1926–E1935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Webster, M.K., Barnett, B.J., Stanchfield, M.L., et al., Stimulation of retinal pigment epithelium with an α7 nAChR agonist leads to Müller glia dependent neurogenesis in the adult mammalian retina, Invest. Ophthalmol. Vis. Sci., 2019, vol. 60, no. 2, pp. 570–579.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Werdich, X.Q., Place, E.M., and Pierce, E.A., Systemic diseases associated with retinal dystrophies, Semin. Ophthalmol., 2014, vol. 29, nos. 5–6, pp. 319–328.

    Article  PubMed  Google Scholar 

  170. Williams, C.J. and Dexter, D.T., Neuroprotective and symptomatic effects of targeting group III mGlu receptors in neurodegenerative disease, J. Neurochem., 2014, vol. 129, no. 1, pp. 4–20.

    Article  CAS  PubMed  Google Scholar 

  171. Winterbourn, C.C. and Kettle, A.J., Redox reactions and microbial killing in the neutrophil phagosome, Antioxid. Redox Signal., 2013, vol. 18, no. 6, pp. 642–660.

    Article  CAS  PubMed  Google Scholar 

  172. Yu, A.L., Fuchshofer, R., Kook, D., et al., Subtoxic oxidative stress induces senescence in retinal pigment epithelial cells via TGF-beta release, Invest. Ophthalmol. Vis. Sci., 2009, vol. 50, no. 2, pp. 926–935.

    Article  PubMed  Google Scholar 

  173. Zacks, D.N., Han, Y., Zeng, Y., et al., Activation of signaling pathways and stress-response genes in an experimental model of retinal detachment, Invest. Ophthalmol. Vis. Sci., 2006, vol. 47, no. 4, pp. 1691–1695.

    Article  PubMed  Google Scholar 

  174. Zacks, D.N., Gene transcription profile of the detached retina (An AOS Thesis), Trans. Am. Ophthalmol. Soc., 2009, vol. 107, pp. 343–382.

  175. Zareba, M., Sarna, T., and Szewczyk, G., Photobleaching of melanosomes from retinal pigment epithelium: II. Effects on the response of living cells to photic stress, Photochem. Photobiol., 2007, vol. 83, no. 4, pp. 925–930.

    Article  CAS  PubMed  Google Scholar 

  176. Zhang, X., Zhang, M., Laties, A.M., et al., Balance of purines may determine life or death of retinal ganglion cells as A3 adenosine receptors prevent loss following P2X7 receptor stimulation, J. Neurochem., 2006, vol. 98, no. 2, pp. 566–575.

    Article  CAS  PubMed  Google Scholar 

  177. Zhang, S.X., Sanders, E., Fliesler, S.J., et al., Endoplasmic reticulum stress and the unfolded protein responses in retinal degeneration, Exp. Eye. Res., 2014, vol. 125, pp. 30–40.

    Article  CAS  PubMed  Google Scholar 

  178. Zhao, X.F., Wan, J., Powell, C., et al., Leptin and IL-6 family cytokines synergize to stimulate Müller glia reprogramming and retina regeneration, Cell Rep., 2014, vol. 9, no. 1, pp. 272–284.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Zhao, L., Zabel, M.K., Wang, X., et al., Microglial phagocytosis of living photoreceptors contributes to inherited retinal degeneration, EMBO Mol. Med., 2015, vol. 7, no. 9, pp. 1179–1197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Zhou, G., Meng, S., Li, Y., et al., Optimal ROS signaling is critical for nuclear reprogramming, Cell Rep., 2016, vol. 15, no. 5, pp. 919–925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the program of the Presidium of the Russian Academy of Sciences “Biodiversity of Natural Systems” within the framework of IDB RUS Government Basic Research Program no. 0108-2018-0005.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu. V. Markitantova.

Ethics declarations

The authors declare that they have no conflict of interest.

This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by A. Barkhash

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Markitantova, Y.V., Simirskii, V.N. Role of the Redox System in Initiation of a Regenerative Response of Neural Eye Tissues in Vertebrates. Russ J Dev Biol 51, 16–30 (2020). https://doi.org/10.1134/S106236042001004X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S106236042001004X

Keywords:

Navigation