Advertisement

Biochemistry (Moscow)

, Volume 83, Issue 11, pp 1318–1331 | Cite as

Molecular Factors of the Maintenance and Activation of the Juvenile Phenotype of Cellular Sources for Eye Tissue Regeneration

  • E. N. GrigoryanEmail author
Review

Abstract

Modern achievements in the understanding of tissue regeneration, identification of endogenous cell sources for regeneration, and development of approaches for induction and differentiation of pluripotent stem cells have open broad prospects for regenerative medicine. However, application of the obtained information in medicine is hindered by insufficient knowledge on the molecular factors and their combinations capable of regulating the age and fate of cellular sources for eye tissue reparation as well as on the regenerative responses of these cells. In the review, we present our own and literature data on cells serving as endogenous sources for eye tissue regeneration in lower and higher vertebrates and properties of gene expression that allow these cells to maintain their juvenile phenotype. Transcription factors and signal pathways providing cell juvenile status as well as cell reprogramming and entry into the S-phase are discussed. The role of systemic factors (blood and immune system factors, hormones, oxidative stress products, and cell rejuvenation factors) in these processes and their interaction with local factors of the cell environment are described. Molecular factors and conditions for induction of reprogramming and proliferation of cellular sources involved in regeneration in vitro are analyzed with special attention to the role of epigenetic factors (associated with cell senescence, in particular) in the source cells conversion during eye tissue regeneration.

Keywords

eye retina eye lens regeneration cell sources transcription factors signaling pathways 

Abbreviations

CMZ

ciliary marginal zone

iPSCs

induced pluripotent stem cells

MG

Müller glia

RPE

retinal pigment epithelium

TH

thyroid hormone

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Grigoryan, E. N. (2016) High regenerative ability of tailed amphibians (Urodela) as a result of the expression of juvenile traits by mature animals, Russ. J. Dev. Biol., 47, 83–92.CrossRefGoogle Scholar
  2. 2.
    Stocum, D. L. (2006) Regenerative Biology and Medicine, Academic Press, Burlington.CrossRefGoogle Scholar
  3. 3.
    Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors, Cell, 126, 663–676.PubMedCrossRefGoogle Scholar
  4. 4.
    Smirnov, S. V. (2006) Metamorphosis in the tailed amphibians: peculiarities, regulation mechanisms, and evolution, Zh. Obshch. Biol., 67, 323–334.PubMedGoogle Scholar
  5. 5.
    Kara, T. C. (1994) Ageing in amphibians, Gerontology, 40, 161–173.PubMedCrossRefGoogle Scholar
  6. 6.
    Eguchi, G., Eguchi, Y., Nakamura, K., Yadav, M. C., Millan, J. L., and Tsonis, P. A. (2011) Regenerative capacity in newts is not altered by repeated regeneration and ageing, Nat. Commun., 2,384.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Maki, N., Suetsugu-Maki, R., Tarui, H., Agata, K., Del Rio-Tsonis, K., and Tsonis, P. A. (2009) Expression of stem cell pluripotency factors during regeneration in newts, Dev. Dyn., 238, 1613–1616.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Maki, N., Suetsugu-Maki, R., Sano, S., Nakamura, K., Nishimura, O., Tarui, H., Del Rio-Tsonis, K., Ohsumi, K., Agata, K., and Tsonis, P. A. (2010) Oocyte-type linker histone B4 is required for transdifferentiation of somatic cells in vivo, FASEB J., 24, 3462–3467.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Stroeva, O. G., and Mitashov, V. I. (1983) Retinal pigment epithelium: proliferation and differentiation during development and regeneration, Int. Rev. Cytol., 83, 221–293.PubMedCrossRefGoogle Scholar
  10. 10.
    Chiba, C., and Mitashov, V. I. (2007) Cellular and molecular events in the adult newt retinal regeneration, in Strategies for Retinal Tissue Repair and Regeneration in Vertebrates: from Fish to Human (Chiba, Ch., ed.), Research Signpost, Kerala, India, pp. 15–33.Google Scholar
  11. 11.
    Grigoryan, E. N. (2015) Competence factors of retinal pigment epithelium cells for reprogramming in the neuronal direction during retinal regeneration in newts, Biol. Bull., 42, 1–11.CrossRefGoogle Scholar
  12. 12.
    Grigoryan, E. N., and Markitantova, Y. V. (2016) Cellular and molecular preconditions for retinal pigment epithelium (RPE) natural reprogramming during retinal regeneration in Urodela, Biomedicines, 4, 10–28.CrossRefGoogle Scholar
  13. 13.
    Luz-Madrigal, A., Grajales-Esquivel, E., McCorkle, A., DiLorenzo, A. M., Barbosa-Sabanero, K., Tsonis, P. A., and Del Rio-Tsonis, K. (2014) Reprogramming of the chick retinal pigmented epithelium after retinal injury, BMC Biol., 12, 28–34.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Perron, M., Kanekar, S., Vetter, M. L., and Harris, W. A. (1998) The genetic sequence of retinal development in the ciliary margin of the Xenopus eye, Dev. Biol., 199, 185–200.PubMedCrossRefGoogle Scholar
  15. 15.
    Miyake, A., and Araki, M. (2014) Retinal stem/progenitor cells in the ciliary marginal zone complete retinal regeneration: a study of retinal regeneration in a novel animal model, Dev. Neurobiol., 74, 739–756.PubMedCrossRefGoogle Scholar
  16. 16.
    Mitashov, V. I., Panova, I. G., and Koussoulakos, C. (2004) Transdifferential potential of ciliary and pigment epithelial cells in lower vertebrates and mammals, Biol. Bull., 31, 324–331.CrossRefGoogle Scholar
  17. 17.
    Fischer, A. J., Bosse, J. L., and El-Hodiri, H. M. (2013) The ciliary marginal zone (CMZ) in development and regeneration of the vertebrate eye, Exp. Eye Res., 116, 199–204.PubMedCrossRefGoogle Scholar
  18. 18.
    Otteson, D. C., and Hitchcock, P. F. (2003) Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration, Vision Res., 43, 927–936.PubMedCrossRefGoogle Scholar
  19. 19.
    Stenkamp, D. L. (2007) Neurogenesis in the fish retina, Int. Rev. Cytol., 259, 173–224.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Grigoryan, E. N. (1998) Cytological Basis of Transdifferentiation in Eye Tissues of Vertebrates: Doctoral (Biol.) Dissertation [in Russian], Institute of Developmental Biology, Russian Academy of Sciences, Moscow.Google Scholar
  21. 21.
    Alunni, A., and Bally-Cuif, L. (2016) A comparative view of regenerative neurogenesis in vertebrates, Development, 143, 741–753.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Okamoto, M., Ohsawa, H., Hayashi, T., Owaribe, K., and Tsonis, P. A. (2007) Regeneration of retinotectal projections after optic tectum removal in adult newts, Mol. Vis., 13, 2112–2118.PubMedGoogle Scholar
  23. 23.
    Joven, A., Morona, R., Gonzalez, A., and Moreno, N. (2013) Expression patterns of Pax6 and Pax7 in the adult brain of a urodele amphibian, Pleurodeles waltl, J. Comp. Neurol., 521, 2088–2124.PubMedCrossRefGoogle Scholar
  24. 24.
    Kaslin, J., Ganz, J., and Brand, M. (2008) Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain, Philos. Trans. R. Soc. Lond. B Biol. Sci., 363, 101–122.PubMedCrossRefGoogle Scholar
  25. 25.
    Engerer, P., Suzuki, S. C., Yoshimatsu, T., Chapouton, P., Obeng, N., Odermatt, B., Williams, P. R., Misgeld, T., and Godinho, L. (2017) Uncoupling of neurogenesis and differentiation during retinal development, EMBO J., 36, 1134–1146.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Sanchez-Farias, A., and Candal, E. (2015) Doublecortin is widely expressed in the developing and adult retina of sharks, Exp. Eye Res., 134, 90–100.PubMedCrossRefGoogle Scholar
  27. 27.
    Grigoryan, E. N., Ivanova, I. P., and Poplinskaya, V. A. (1996) Discovery of new internal sources of the neural retina regeneration after its detachment in newts. I. Morphological and quantitative studies, Izv. Akad. Nauk, Ser. Biol., 3, 319–332.Google Scholar
  28. 28.
    Grigoryan, E. N. (2007) Alternative intrinsic cell sources for neural retina regeneration in adult urodelean amphibians, in Strategies for Retinal Tissue Repair and Regeneration in Vertebrates: from Fish to Human (Chiba, Ch., ed.), Research Signpost, Kerala, India, pp. 35–62.Google Scholar
  29. 29.
    Martinez-Navarrete, G. C., Angulo, A., and Cuenca, N. (2008) Gradual morphogenesis of retinal neurons in the peripheral retinal margin of adult monkeys and humans, J. Comp. Neurol., 511, 557–580.PubMedCrossRefGoogle Scholar
  30. 30.
    Goldman, D. (2014) Müller glial cell reprogramming and retina regeneration, Nat. Rev. Neurosci., 15, 431–442.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Hamon, A., Roger, J. E., Yang, X. J., and Perron, M. (2016) Müller glial cell-dependent regeneration of the neural retina: an overview across vertebrate model systems, Dev. Dyn., 245, 727–738.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Lenkowski, J. R., and Raymond, P. A. (2014) Müller glia: stem cells for generation and regeneration of retinal neurons in teleost fish, Prog. Retin. Eye Res., 40, 94–123.PubMedCrossRefGoogle Scholar
  33. 33.
    Fischer, A. J., McGuire, C. R., Dierks, B. D., and Reh, T. A. (2002) Insulin and fibroblast growth factor 2 activate a neurogenic program in Müller glia of the chicken retina, J. Neurosci., 22, 9387–9398.PubMedCrossRefGoogle Scholar
  34. 34.
    Fischer, A. J., and Reh, T. A. (2002) Exogenous growth factors stimulate the regeneration of ganglion cells in the chicken retina, Dev. Biol., 251, 367–379.PubMedCrossRefGoogle Scholar
  35. 35.
    Jorstad, N. L., Wilken, M. S., Grimes, W. N., Wohl, S. G., Vanden Bosch, L. S., Yoshimatsu, T., Wong, R. O., Rieke, F., and Reh, T. A. (2017) Stimulation of functional neuronal regeneration from Müller glia in adult mice, Nature, 548, 103–107.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Bernardos, R. L., Barthel, L. K., Meyers, J. R., and Raymond, P. A. (2007) Late-stage neuronal progenitors in the retina are radial Müller glia that functions as retinal stem cells, J. Neurosci., 27, 7028–7040.PubMedCrossRefGoogle Scholar
  37. 37.
    Lewis, G. P., Chapin, E. A., Luna, G., Linberg, K. A., and Fisher, S. K. (2010) The fate of Müller’s glia following experimental retinal detachment: nuclear migration, cell division, and subretinal glial scar formation, Mol. Vis., 16, 1361–1372.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Kimura, Y., Madhavan, M., Call, M. K., Santiago, W., Tsonis, P. A., Lambris, J. D., and Del Rio-Tsonis, K. (2003) Expression of complement 3 and complement 5 in newt limb and lens regeneration, J. Immunol., 170, 2331–2339.PubMedCrossRefGoogle Scholar
  39. 39.
    Imokawa, Y., Simon, A., and Brockes, J. P. (2004) Critical role for thrombin in vertebrate lens regeneration, Philos. Trans. R. Soc. Lond. B Biol. Sci., 359, 765–776.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Godwin, J. W., and Brockes, J. P. (2006) Regeneration, tissue injury and the immune response, J. Anat., 209, 423–432.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Godwin, J. W., Pinto, A. R., and Rosenthal, N. A. (2017) Chasing the recipe for a pro-regenerative immune system, Semin. Cell Dev. Biol., 61, 71–79.PubMedCrossRefGoogle Scholar
  42. 42.
    London, A., Itskovich, E., Benhar, I., Kalchenko, V., Mack, M., Jung, S., and Schwartz, M. (2011) Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages, J. Exp. Med., 208, 23–39.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Erler, P., and Monaghan, J. R. (2015) The link between injury-induced stress and regenerative phenomena: a cellular and genetic synopsis, Biochim. Biophys. Acta, 1849, 454–461.PubMedCrossRefGoogle Scholar
  44. 44.
    Hameed, L. S., Berg, D. A., Belnoue, L., Jensen, L. D., Cao, Y., and Simon, A. (2015) Environmental changes in oxygen tension reveal ROS-dependent neurogenesis and regeneration in the adult newt brain, eLife, 4, e08422.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Wu, W. C., Hu, D. N., Gao, H. X., Chen, M., Wang, D., Rosen, R., and McCormick, S. A. (2010) Subtoxic levels hydrogen peroxide-induced production of interleukin-6 by retinal pigment epithelial cells, Mol. Vis., 161, 864–873.Google Scholar
  46. 46.
    Echeverri-Ruiz, N., Haynes, T., Landers, J., Woods, J., Gemma, M. J., Hughes, M., and Del Rio-Tsonis, K. (2018) A biochemical basis for induction of retina regeneration by antioxidants, Dev. Biol., 433, 394–403.PubMedCrossRefGoogle Scholar
  47. 47.
    Neroev, V. V., Archipova, M. M., Bakeeva, L. E., Fursova, A. Zh., Grigorian, E. N., Grishanova, A. Y., Iomdina, E. N., Ivashchenko, Zh. N., Katargina, L. A., Khoroshilova-Maslova, I. P., Kilina, O. V., Kolosova, N. G., Kopenkin, E. P., Korshunov, S. S., Kovaleva, N. A., Novikova, Yu. P., Philippov, P. P., Pilipenko, D. I., Robustova, A. V., Saprunova, V. B., Senin, I. I., Skulachev, M. V., Sotnikova, L. F., Stefanova, N. A., Tihomirova, N. K., Tsapenko, I. V., Shchipanova, A. I., Zinovkin, R. A., and Skulachev, V. P. (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 4. Age-related eye disease. SkQ1 returns vision to blind animals, Biochemistry (Moscow), 73, 1317–1328.CrossRefGoogle Scholar
  48. 48.
    Grigoryan, E. N., Novikova, Y. P., Gancharova, O. S., Kilina, O. V., and Philippov, P. P. (2012) New antioxidant SkQ1 is an effective protector of rat eye retinal pigment epithelium and choroid under conditions of long-term organotypic cultivation, Adv. Aging Res., 1, 31–37.CrossRefGoogle Scholar
  49. 49.
    Novikova, Yu. P., Gancharova, O. S., Eichler, O. V., Philippov, P. P., and Grigoryan, E. N. (2013) Preventive and therapeutic effects of SkQ1 containing Visomitin eye drops against light induced retinal degeneration, Biochemistry (Moscow), 79, 1101–1110.CrossRefGoogle Scholar
  50. 50.
    Hayes, S., Nelson, B. R., Buckingham, B., and Reh, T. A. (2007) Notch signaling regulates regeneration in the avian retina, Dev Biol., 312, 300–311.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Osakada, F., Ooto, S., Akagi, T., Mandai, M., Akaike, A., and Takahashi, M. (2007) Wnt signaling promotes regeneration in the retina of adult mammals, J. Neurosci., 27, 4210–4219.PubMedCrossRefGoogle Scholar
  52. 52.
    Hayashi, T., Mizuno, N., Owaribe, K., Kuroiwa, A., and Okamoto, M. (2002) Regulated lens regeneration from isolated pigmented epithelial cells of newt iris in culture in response to FGF2/4, Differentiation, 70, 101–108.PubMedCrossRefGoogle Scholar
  53. 53.
    Hayashi, T., Mizuno, N., Ueda, Y., Okamoto, M., and Kondoh, H. (2004) FGF2 triggers iris-derived lens regeneration in newt eye, Mech. Dev., 121, 519–526.PubMedCrossRefGoogle Scholar
  54. 54.
    Hayashi, T., Mizuno, N., Takada, R., Takada, S., and Kondoh, H. (2006) Determinative role of Wnt signals in dorsal iris-derived lens regeneration in newt eye, Mech. Dev., 123, 793–800.PubMedCrossRefGoogle Scholar
  55. 55.
    Markitantova, Yu. V., Avdonin, P. P., and Grigoryan, E. N. (2014) FGF2 signaling pathway components in tissues of the posterior eye sector in the adult newt Pleurodeles waltl, Biol. Bull., 41, 297–305.CrossRefGoogle Scholar
  56. 56.
    Borday, C., Cabochette, P., Parain, K., Mazurier, N., Janssens, S., Tran, H. T., Sekkali, B., Bronchain, O., Vleminckx, K., Locker, M., and Perron, M. (2012) Antagonistic cross-regulation between Wnt and Hedgehog signaling pathways controls post-embryonic retinal proliferation, Development, 139, 3499–3509.PubMedCrossRefGoogle Scholar
  57. 57.
    Todd, L., Suarez, L., Quinn, C., and Fischer, A. J. (2017) Retinoic acid-signaling regulates the proliferative and neurogenic capacity of Müller glia-derived progenitor cells in the avian retina, Stem Cells, 65, 1640–1655.Google Scholar
  58. 58.
    Raymond, P. A., Barthel, L. R., Bernardos, R. L., and Perkowski, J. J. (2006) Molecular characterization of retinal stem cells and their niches in adult zebrafish, BMC Dev. Biol., 6,36.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Das, A. V., Mallya, K. B., Zhao, X., Ahmad, F., Bhattacharya, S., Thoreson, W. B., Hegde, G. V., and Ahmad, I. (2006) Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling, Dev. Biol., 299, 283–302.PubMedCrossRefGoogle Scholar
  60. 60.
    Denayer, T., Locker, M., Borday, C., Deroo, T., Janssens, S., Hecht, A., van Roy, F., Perron, M., and Vleminck, K. (2008) Canonical Wnt signaling controls proliferation of retinal stem/progenitor cells in postembryonic Xenopus eyes, Stem Cells, 8, 2063–2074.CrossRefGoogle Scholar
  61. 61.
    Del Debbio, C. B., Balasubramanian, S., Parameswaran, S., Chaudhuri, A., Qiu, F., and Ahmad, I. (2010) Notch and Wnt signaling mediated rod photoreceptor regeneration by Müller cells in adult mammalian retina, PLoS One, 5, e12425.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Aurora, A. B., and Olson, E. N. (2014) Immune modulation of stem cells and regeneration, Cell Stem Cell, 15, 14–25.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Faunes, F., Gundermann, D. G., Munoz, R., Bruno, R., and Larrain, J. (2017) The heterochronic gene Lin28 regulates amphibian metamorphosis through disturbance of thyroid hormone function, Dev. Biol., 425, 142–151.PubMedCrossRefGoogle Scholar
  64. 64.
    Gallina, D., Zelinka, Ch., and Fischer, A. J. (2014) Glucocorticoid receptors in the retina, Müller glia and the formation of Muller glia-derived progenitors, Development, 141, 3340–3351.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Mescher, A. L. (2017) Macrophages and fibroblasts during inflammation and tissue repair in models of organ regeneration, Regeneration (Oxf.), 4, 39–53.CrossRefGoogle Scholar
  66. 66.
    Hui, S. P., Sheng, D. Z., Sugimoto, K., Gonzalez-Rajal, A., Nakagawa, S., Hesselson, D., and Kikuchi, K. (2017) Zebrafish regulatory T cells mediate organ-specific regenerative programs, Dev. Cell, 43, 659–672.PubMedCrossRefGoogle Scholar
  67. 67.
    Haynes, T., Luz-Madrigal, A., Reis, E. S., Echeverri Ruiz, N. P., Grajales-Esquivel, E., Tzekou, A., Tsonis, P. A., Lambris, J. D., and Del Rio-Tsonis, K. (2013) Complement anaphylatoxin C3a is a potent inducer of embryonic chick retina regeneration, Nat. Commun., 4, 2312.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Godwin, J. W., Pinto, A. R., and Rosenthal, N. A. (2017) Chasing the recipe for a pro-regenerative immune system, Semin. Cell Dev. Biol., 61, 71–79.PubMedCrossRefGoogle Scholar
  69. 69.
    Bitto, A., and Kaeberlein, M. (2014) Rejuvenation: it is in our blood? Cell Metabolism, 20, 2–4.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Rochette, L., and Vergely, C. (2016) “Pro-youthful” factors in the labyrinth of cardiac rejuvenation, Exp. Gerontol., 83, 1–5.PubMedCrossRefGoogle Scholar
  71. 71.
    Hanoki, K. (2017) Preventing aging with stem cell rejuvenation: feasible or infeasible? World J. Stem Cells, 26, 1–8.CrossRefGoogle Scholar
  72. 72.
    Smith, L. K., White, Ch. W., 3rd., and Villeda, S. A. (2018) The systemic environment: at the interface of aging and adult neurogenesis, Cell Tissue Res., 371, 105–113.PubMedCrossRefGoogle Scholar
  73. 73.
    Andersen, R. E., and Lim, D. A. (2014) An ingredient for the elixir of youth, Cell Res., 24, 1381–1382.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Katsimpardi, L., Litterman, N. K., Schein, P. A., Miller, C. M., Loffredo, F. S., Wojtkiewicz, G. R., Chen, J. W., Lee, R. T., Wagers, A. J., and Rubin, L. L. (2014) Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors, Science, 344, 630–634.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Elabd, C., Cousin, W., Upadhyayula, P., Chen, R. Y., Chooljian, M. S., Li, J., Kung, S., Jiang, K. P., and Conboy, I. M. (2014) Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration, Nat. Commun., 5, 4082.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Conover, J. C. (2008) The neural stem cell niche, Cell Tissue Res., 331, 211–224.PubMedCrossRefGoogle Scholar
  77. 77.
    Villeda, S. A., Luo, J., Mosher, K. I., Zou, B., Britschgi, M., Bieri, G., Stan, T. M., Fainberg, N., Ding, Z., Eggel, A., Lucin, K. M., Czirr, E., Park, J.-S., Couillard-Despres, S., Aigner, L., Li, G., Peskind, E. R., Kaye, J. A., Quinn, J. F., Galasko, D. R., Xie, X. S., Rando, T. A., and Wyss-Coray, T. (2012) The ageing systemic milieu negatively regulates neurogenesis and cognitive function, Nature, 477, 90–94.CrossRefGoogle Scholar
  78. 78.
    Villeda, S. A., Plambeck, K. E., Middeldorp, J., Castellano, J. M., Mosher, K. I., Luo, J., Smith, L. K., Bieri, G., Lin, K., Berdnik, D., Wabl, R., Udeochu, J., Wheatley, E. G., Zou, B., Simmons, D. A., Xie, X. S., Longo, F. M., and Wyss-Coray, T. (2014) Young blood reverses age-related impairments in cognitive function and synaptic plasticity in mice, Nat. Med., 20, 659–663.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Powell, C., Grant, A. R., Cornblath, E., and Goldman, D. (2013) Analysis of DNA methylation reveals a partial reprogramming of the Muller glia genome during retina regeneration, Proc. Natl. Acad. Sci. USA, 110, 19814–19819.PubMedCrossRefGoogle Scholar
  80. 80.
    Gaspar-Maia, A., Alajem, A., Meshorer, E., and Ramalho-Santos, M. (2011) Open chromatin in pluripotency and reprogramming, Nat. Rev. Mol. Cell Biol., 12, 36–47.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Polo, J. M., Anderssen, E., Walsh, R. M., Schwarz, B. A., Nefzger, C. M., Lim, S. M., Borkent, M., Apostolou, E., Alaei, S., Cloutier, J., Bar-Nur, O., Cheloufi, S., Stadtfeld, M., Figueroa, M. E., Robinton, D., Natesan, S., Melnick, A., Zhu, J., Ramaswamy, S., and Hochedlinger, K. (2012) A molecular roadmap of reprogramming somatic cells into iPS cells, Cell, 151, 1617–1632.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Maki, N., Tsonis, P. A., and Agata, K. (2010) Changes in global histone modifications during dedifferentiation in newt lens regeneration, Mol. Vis., 16, 1893–1897.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Maki, N., Martinson, J., Nishimura, O., Tarui, H., Meller, J., Tsonis, P. A., and Agata, K. (2010) Expression profiles during dedifferentiation in newt lens regeneration revealed by expressed sequence tags, Mol. Vis., 16, 72–78.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Markitantova, Yu. V., Avdonin, P. P., and Grigoryan, E. N. (2015) Identification of the gene encoding nucleostemin in the eye tissues of Pleurodeles waltl, Biol. Bull., 42, 379–386.CrossRefGoogle Scholar
  85. 85.
    Srivastava, D., and DeWitt, N. (2016) In vivo cellular reprogramming: the next generation, Cell, 166, 1386–1396.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Vierbuchen, T., Ostermeier, A., Pang, Z. P., Kokubu, Y., Sudhof, T. C., and Wernig, M. (2010) Direct conversion of fibroblasts to functional neurons by defined factors, Nature, 463, 1035–1041.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Niu, W., Zang, T., Zou, Y., Fang, S., Smith, D. K., Bachoo, R., and Zhang, C. L. (2013) In vivo reprogramming of astrocytes to neuroblasts in the adult brain, Nat. Cell Biol., 15, 1164–1175.PubMedCrossRefGoogle Scholar
  88. 88.
    Kuznetsova, A. V., Milyushina, L. A., Mikaelyan, A. S., Zinov’eva, R. D., Grigoryan, E. N., and Aleksandrova, M. A. (2010) Dedifferentiation of retinal pigment epithelium cells form adult human eye in vitro, Mol. Med., 6, 23–29.Google Scholar
  89. 89.
    Kuznetsova, A. V., Grigoryan, E. N., and Aleksandrova, M. A. (2011) Human adult retinal pigment epithelium cells as potential cell source for retina recovery, Cell Tiss. Biol., 5, 495–502.CrossRefGoogle Scholar
  90. 90.
    Kuznetsova, A. V., Kurinov, A. M., and Aleksandrova, M. A. (2014) Cell models to study regulation of cell transformation in pathologies of retinal pigment epithelium, J. Ophthalmol., 2014, 801787.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Milyushina, L. A., Kuznetsova, A. V., Grigoryan, E. N., and Aleksandrova, M. A. (2011) Phenotypic plasticity of retinal pigment epithelial cells from adult human eye in vitro, Bull. Exp. Biol. Med., 151, 506–511.PubMedCrossRefGoogle Scholar
  92. 92.
    Milyushina, L. A., Verdiev, B. I., Kuznetsova, A. V., and Aleksandrova, M. A. (2012) Expression of multipotent and retinal markers in pigment epithelium of adult human in vitro, Bull. Exp. Biol. Med., 163, 157–162.CrossRefGoogle Scholar
  93. 93.
    Shafei, E. V., Kurinov, A. M., Kuznetsova, A. V., and Aleksandrova, M. A. (2017) Reprogramming of human retinal pigment epithelial cells under the effect of bFGF in vitro, Bull. Exp. Biol. Med., 163, 574–582.PubMedCrossRefGoogle Scholar
  94. 94.
    Salero, E., Blenkinsop, T. A., Corneo, B., Harris, A., Rabin, D., Stern, J. H., and Temple, S. (2012) Adult human RPE can be activated into a multipotent stem cell that produces mesenchymal derivatives, Cell Stem Cell, 10, 88–95.PubMedCrossRefGoogle Scholar
  95. 95.
    Tropepe, V., Coles, B. L., Chiasson, B. J., Horsford, D. J., Elia, A. J., McInnes, R. R., and van der Kooy, D. (2000) Retinal stem cells in the adult mammalian eye, Science, 287, 2032–2036.PubMedCrossRefGoogle Scholar
  96. 96.
    Cicero, S. A., Johnson, D., Reyntjens, S., Frase, Sh., Connell, S., Chow, L. M. L., Baker, S. J., Sorrentino, B. P., and Dyer, M. A. (2009) Cells previously identified as retinal stem cells are pigmented ciliary epithelial cells, Proc. Natl. Acad. Sci. USA, 106, 6685–6690.PubMedCrossRefGoogle Scholar
  97. 97.
    Engelhardt, M., Bogdahn, U., and Aigner, L. (2005) Adult retinal pigment epithelium cells express neural progenitor properties and the neuronal precursor protein doublecortin, Brain Res., 1040, 98–111.PubMedCrossRefGoogle Scholar
  98. 98.
    Nakamura, K., Rafiqul, M. R., Takayanagi, M., Yasumuro, H., Inami, W., Kunahong, A., Casco-Robles, R. M., Toyama, F., and Chiba, C. (2014) A transcriptome for the study of early processes of retinal regeneration in the adult newt, Cynops pyrrhogaster, PLoS One, 9, e10983.Google Scholar
  99. 99.
    Pollak, J., Wilken, M. S., Ueki, Y., Cox, K. E., Sullivan, J. M., Taylor, R. J., Levine, E. M., and Reh, T. A. (2013) ASCL1 reprograms mouse Müller glia into neurogenic retinal progenitors, Development, 140, 2619–2631.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Angbohang, A., Wu, N., Charalambous, T., Eastlake, K., Lei, Y., Kim, Y. S., Sun, X. H., and Limb, G. A. (2016) Downregulation of the canonical WNT signaling pathway by TGFβ1 inhibits photoreceptor differentiation of adult human Müller glia with stem cell characteristics, Stem Cells Dev., 25, 1–12.PubMedCrossRefGoogle Scholar
  101. 101.
    Bhatia, B., Singhal, S., Lawrence, J. M., Khaw, P. T., and Limb, G. A. (2009) Distribution of Müller stem cells within the neural retina: evidence for the existence of a ciliary margin-like zone in the adult human eye, Exp. Eye Res., 89, 373–382.PubMedCrossRefGoogle Scholar
  102. 102.
    Bhatia, B., Jayaram, H., Singhal, S., Jones, M. F., and Limb, G. A. (2011) Differences between the neurogenic and proliferative abilities of Müller glia with stem cell characteristics and the ciliary epithelium from the adult human eye, Exp. Eye Res., 93, 852–861.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Xu, N., Chen, Y., Dean, K. C., Lu, X., Liu, X., Wang, W., Dean, D. C., Kaplan, H. J., Gao, L., Dong, F., and Liu, Y. (2017) Sphere-induced rejuvenation of swine and human Müller glia is primarily caused by telomere elongation, Stem Cells, 6, 1579–1591.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Koltsov Institute of Developmental BiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations