DOI QR코드

DOI QR Code

Advances in research to restore vision

  • Received : 2023.01.17
  • Accepted : 2023.02.08
  • Published : 2023.03.31

Abstract

Mammalian eyes have a limited ability to regenerate once neurons degenerate. This results in visual impairment that impacts the quality of life among adult populations as well as in young children leading to lifelong consequences. Various therapies are in development to restore vision, and these include gene therapy, stem cell therapy, in-vivo transdifferentiation, and transplantation of a patient's whole eye obtained from interspecies blastocyst complementation. This review discusses advances in the research as well as hurdles that need to be resolved to have a successful restoration of vision.

Keywords

References

  1. Almasieh M, Wilson AM, Morquette B, Cueva Vargas JL, Di Polo A. 2012. The molecular basis of retinal ganglion cell death in glaucoma. Prog. Retin. Eye Res. 31:152-181. https://doi.org/10.1016/j.preteyeres.2011.11.002
  2. Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, Chen PJ, Wilson C, Newby GA, Raguram A, Liu DR. 2019. Search-and-replace genome editing without doublestrand breaks or donor DNA. Nature 576:149-157. https://doi.org/10.1038/s41586-019-1711-4
  3. Ballard EB and Wu J. 2021. Growth competition in interspecies chimeras: a new paradigm for blastocyst complementation. Cell Stem Cell 28:3-5. https://doi.org/10.1016/j.stem.2020.12.011
  4. Barber AC, Hippert C, Duran Y, West EL, Bainbridge JW, WarreCornish K, Luhmann UF, Lakowski J, Sowden JC, Ali RR, Pearson RA. 2013. Repair of the degenerate retina by photoreceptor transplantation. Proc. Natl. Acad. Sci. U. S. A. 110: 354-359. https://doi.org/10.1073/pnas.1212677110
  5. Botto C, Rucli M, Tekinsoy MD, Pulman J, Sahel JA, Dalkara D. 2022. Early and late stage gene therapy interventions for inherited retinal degenerations. Prog. Retin. Eye Res. 86:100975.
  6. Bourne D, Li Y, Komatsu C, Miller MR, Davidson EH, He L, Rosner IA, Tang H, Chen W, Solari MG, Schuman JS, Washington KM. 2017. Whole-eye transplantation: a look into the past and vision for the future. Eye (Lond.) 31:179-184. https://doi.org/10.1038/eye.2016.272
  7. Brody BL, Gamst AC, Williams RA, Smith AR, Lau PW, Dolnak D, Rapaport MH, Kaplan RM, Brown SI. 2001. Depression, visual acuity, comorbidity, and disability associated with agerelated macular degeneration. Ophthalmology 108:1893-1901. https://doi.org/10.1016/S0161-6420(01)00754-0
  8. Carr AJ, Vugler AA, Hikita ST, Lawrence JM, Gias C, Chen LL, Buchholz DE, Ahmado A, Semo M, Smart MJ, Hasan S, da Cruz L, Johnson LV, Clegg DO, Coffey PJ. 2009. Protective effects of human iPS-derived retinal pigment epithelium cell transplantation in the retinal dystrophic rat. PLoS One 4: e8152.
  9. Chen J, Lansford R, Stewart V, Young F, Alt FW. 1993. RAG2-deficient blastocyst complementation: an assay of gene function in lymphocyte development. Proc. Natl. Acad. Sci. U. S. A. 90:4528-4532. https://doi.org/10.1073/pnas.90.10.4528
  10. De Los Angeles A, Wu J. 2022. New concepts for generating interspecies chimeras using human pluripotent stem cells. Protein Cell 13:234-238. https://doi.org/10.1007/s13238-021-00880-5
  11. Evans MJ and Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154-156. https://doi.org/10.1038/292154a0
  12. Freedman BS. 2018. Hopes and difficulties for blastocyst complementation. Nephron 138:42-47. https://doi.org/10.1159/000480370
  13. Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR. 2017. Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage. Nature 551: 464-471. (Erratum published 2018, Nature 559:E8)
  14. GBD 2019 Blindness and Vision Impairment Collaborators and Vision Loss Expert Group of the Global Burden of Disease Study. 2021. Trends in prevalence of blindness and distance and near vision impairment over 30 years: an analysis for the Global Burden of Disease Study. Lancet Glob. Health 9:e130-e143. https://doi.org/10.1016/S2214-109X(20)30425-3
  15. Gilbert C and Awan H. 2003. Blindness in children. BMJ 327: 760-761. https://doi.org/10.1136/bmj.327.7418.760
  16. Hartong DT, Berson EL, Dryja TP. 2006. Retinitis pigmentosa. Lancet 368:1795-1809. https://doi.org/10.1016/S0140-6736(06)69740-7
  17. Hastie E and Samulski RJ. 2015. Adeno-associated virus at 50: a golden anniversary of discovery, research, and gene therapy success--a personal perspective. Hum. Gene Ther. 26:257-265. https://doi.org/10.1089/hum.2015.025
  18. Kobayashi T, Yamaguchi T, Hamanaka S, Kato-Itoh M, Yamazaki Y, Ibata M, Sato H, Lee YS, Usui J, Knisely AS, Hirabayashi M, Nakauchi H. 2010. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell 142:787-799. https://doi.org/10.1016/j.cell.2010.07.039
  19. Lamba DA, Gust J, Reh TA. 2009. Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell Stem Cell 4:73-79. https://doi.org/10.1016/j.stem.2008.10.015
  20. Lamba DA, Karl MO, Ware CB, Reh TA. 2006. Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 103:12769-12774. https://doi.org/10.1073/pnas.0601990103
  21. Lamba DA, McUsic A, Hirata RK, Wang PR, Russell D, Reh TA. 2010. Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells. PLoS One 5:e8763.
  22. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. 2000. Lens injury stimulates axon regeneration in the mature rat optic nerve. J. Neurosci. 20:4615-4626. https://doi.org/10.1523/JNEUROSCI.20-12-04615.2000
  23. Loriaut P, Loriaut P, Boyer P, Massin P, Cochereau I. 2014. Visual impairment and hip fractures: a case-control study in elderly patients. Ophthalmic Res. 52:212-216. https://doi.org/10.1159/000362881
  24. Lu Y, Brommer B, Tian X, Krishnan A, Meer M, Wang C, Vera DL, Zeng Q, Yu D, Bonkowski MS, Yang JH, Zhou S, Hoffmann EM, Karg MM, Schultz MB, Kane AE, Davidsohn N, Korobkina E, Chwalek K, Rajman LA, Church GM, Hochedlinger K, Gladyshev VN, Horvath S, Levine ME, Gregory-Ksander MS, Ksander BR, He Z, Sinclair DA. 2020. Reprogramming to recover youthful epigenetic information and restore vision. Nature 588:124-129. https://doi.org/10.1038/s41586-020-2975-4
  25. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, Akimoto M, Swaroop A, Sowden JC, Ali RR. 2006. Retinal repair by transplantation of photoreceptor precursors. Nature 444:203-207. https://doi.org/10.1038/nature05161
  26. Maheshwari A and Finger PT. 2018. Cancers of the eye. Cancer Metastasis Rev. 37:677-690. https://doi.org/10.1007/s10555-018-9762-9
  27. Marchesi N, Fahmideh F, Boschi F, Pascale A, Barbieri A. 2021. Ocular neurodegenerative diseases: interconnection between retina and cortical areas. Cells 10:2394.
  28. Meyer JS, Katz ML, Maruniak JA, Kirk MD. 2006. Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells 24:274-283. https://doi.org/10.1634/stemcells.2005-0059
  29. Moore DL, Blackmore MG, Hu Y, Kaestner KH, Bixby JL, Lemmon VP, Goldberg JL. 2009. KLF family members regulate intrinsic axon regeneration ability. Science 326:298-301. https://doi.org/10.1126/science.1175737
  30. Muller A, Hauk TG, Fischer D. 2007. Astrocyte-derived CNTF switches mature RGCs to a regenerative state following inflammatory stimulation. Brain 130:3308-3320. https://doi.org/10.1093/brain/awm257
  31. Nishimura T, Suchy FP, Bhadury J, Igarashi KJ, Charlesworth CT, Nakauchi H. 2021. Generation of functional organs using a cell-competitive niche in intra- and inter-species rodent chimeras. Cell Stem Cell 28:141-149.e3. https://doi.org/10.1016/j.stem.2020.11.019
  32. Pearson RA, Gonzalez-Cordero A, West EL, Ribeiro JR, Aghaizu N, Goh D, Sampson RD, Georgiadis A, Waldron PV, Duran Y, Naeem A, Kloc M, Cristante E, Kruczek K, Warre-Cornish K, Sowden JC, Smith AJ, Ali RR. 2016. Donor and host photoreceptors engage in material transfer following transplantation of post-mitotic photoreceptor precursors. Nat. Commun. 7:13029.
  33. Ratican SE, Osborne A, Martin KR. 2018. Progress in gene therapy to prevent retinal ganglion cell loss in glaucoma and Leber's hereditary optic neuropathy. Neural Plast. 2018: 7108948.
  34. Santos-Ferreira T, Llonch S, Borsch O, Postel K, Haas J, Ader M. 2016. Retinal transplantation of photoreceptors results in donor-host cytoplasmic exchange. Nat. Commun. 7:13028.
  35. Sher H. 1981. Revascularization of autotransplanted ovine eyes by microsurgical anastomosis. J. Microsurg. 2:269-272. https://doi.org/10.1002/micr.1920020408
  36. Shi J, Ellenberg D, Kim JY, Qian H, Ripps H, Jain S, Chang JH, Azar DT. 2009. Restoration of electroretinogram activity in exenterated swine eyes following ophthalmic artery anastomosis. Restor. Neurol. Neurosci. 27:351-357. https://doi.org/10.3233/RNN-2009-0485
  37. Singh MS, Balmer J, Barnard AR, Aslam SA, Moralli D, Green CM, Barnea-Cramer A, Duncan I, MacLaren RE. 2016. Transplanted photoreceptor precursors transfer proteins to host photoreceptors by a mechanism of cytoplasmic fusion. Nat. Commun. 7:13537.
  38. Stone LS and Cole CH. 1943. Grafted eyes of young and old adult salamanders (Amblystoma punctatum) showing return of vision. Yale J. Biol. Med. 15:735-754.2.
  39. Stone LS and Ellison FS. 1945. Return of vision in eyes exchanged between adult salamanders of different species. J. Exp. Zool. 100:217-227. https://doi.org/10.1002/jez.1401000205
  40. 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. https://doi.org/10.1016/j.cell.2006.07.024
  41. van Lookeren Campagne M, LeCouter J, Yaspan BL, Ye W. 2014. Mechanisms of age-related macular degeneration and therapeutic opportunities. J. Pathol. 232:151-164. https://doi.org/10.1002/path.4266
  42. Venugopalan P, Wang Y, Nguyen T, Huang A, Muller KJ, Goldberg JL. 2016. Transplanted neurons integrate into adult retinas and respond to light. Nat. Commun. 7:10472.
  43. Wang L, Zhu Z, Scheetz J, He M. 2021. Visual impairment and ten-year mortality: the Liwan Eye Study. Eye (Lond.) 35:2173-2179. https://doi.org/10.1038/s41433-020-01226-x
  44. Wan J and Goldman D. 2016. Retina regeneration in zebrafish. Curr. Opin. Genet. Dev. 40:41-47. https://doi.org/10.1016/j.gde.2016.05.009
  45. Wawersik S and Maas RL. 2000. Vertebrate eye development as modeled in Drosophila. Hum. Mol. Genet. 9:917-925. https://doi.org/10.1093/hmg/9.6.917
  46. Wong EY, Chou SL, Lamoureux EL, Keeffe JE. 2008. Personal costs of visual impairment by different eye diseases and severity of visual loss. Ophthalmic Epidemiol. 15:339-344. https://doi.org/10.1080/09286580802227394
  47. Wong TY, Cheung CM, Larsen M, Sharma S, Simo R. 2016. Diabetic retinopathy. Nat. Rev. Dis. Primers 2:16012.
  48. Wu J, Platero-Luengo A, Sakurai M, Sugawara A, Gil MA, Yamauchi T, Suzuki K, Bogliotti YS, Cuello C, Morales Valencia M, Okumura D, Luo J, Vilarino M, Parrilla I, Soto DA, Martinez CA, Hishida T, Sanchez-Bautista S, Martinez-Martinez ML, Wang H, Nohalez A, Aizawa E, Martinez-Redondo P, Ocampo A, Reddy P, Roca J, Maga EA, Esteban CR, Berggren WT, Nunez Delicado E, Lajara J, Guillen I, Guillen P, Campistol JM, Martinez EA, Ross PJ, Izpisua Belmonte JC. 2017. Interspecies chimerism with mammalian pluripotent stem cells. Cell 168:473-486.e15. https://doi.org/10.1016/j.cell.2016.12.036
  49. Xiao D, Jin K, Qiu S, Lei Q, Huang W, Chen H, Su J, Xu Q, Xu Z, Gou B, Tie X, Liu F, Liu S, Liu Y, Xiang M. 2021. In vivo regeneration of ganglion cells for vision restoration in mammalian retinas. Front. Cell Dev. Biol. 9:755544.
  50. Xie Y and Chen B. 2022. Critical examination of Muller gliaderived in vivo neurogenesis in the mouse retina. Front. Cell Dev. Biol. 10:830382.
  51. Yamaguchi T, Sato H, Kato-Itoh M, Goto T, Hara H, Sanbo M, Mizuno N, Kobayashi T, Yanagida A, Umino A, Ota Y, Hamanaka S, Masaki H, Rashid ST, Hirabayashi M, Nakauchi H. 2017. Interspecies organogenesis generates autologous functional islets. Nature 542:191-196. https://doi.org/10.1038/nature21070
  52. Yao K, Qiu S, Wang YV, Park SJH, Mohns EJ, Mehta B, Liu X, Chang B, Zenisek D, Crair MC, Demb JB, Chen B. 2018. Restoration of vision after de novo genesis of rod photoreceptors in mammalian retinas. Nature 560:484-488. https://doi.org/10.1038/s41586-018-0425-3
  53. Yin Y, De Lima S, Gilbert HY, Hanovice NJ, Peterson SL, Sand RM, Sergeeva EG, Wong KA, Xie L, Benowitz LI. 2019. Optic nerve regeneration: a long view. Restor. Neurol. Neurosci. 37:525-544. https://doi.org/10.3233/rnn-190960
  54. Zhang CJ, Ma Y, Jin ZB. 2021. The road to restore vision with photoreceptor regeneration. Exp. Eye Res. 202:108283.
  55. Zheng C, Ballard EB, Wu J. 2021. The road to generating transplantable organs: from blastocyst complementation to interspecies chimeras. Development 148:dev195792.