Immunosuppression via Loss of IL2rγ Enhances Long-Term Functional Integration of hESC-Derived Photoreceptors in the Mouse Retina

Cell Stem Cell

Volumn 20, Issue 3, 2017, Pages 374-384.e5

  Zhu, Jie ^a   Cifuentes, Helen ^a   Reynolds, Joseph ^a   Lamba, Deepak A ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

AMD; c Fos; immune rejection; iPSC; Leber congenital amaurosis; natural killer cells; pupillary light reflex; retinitis pigmentosa; stem cells; visual function

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; HISTONE H3; INTERLEUKIN 2 RECEPTOR GAMMA; OPSIN; TRANSCRIPTION FACTOR OTX2; BIOLOGICAL MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CELL TRANSPLANTATION; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; IMMEDIATE EARLY GENE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; LONG TERM SURVIVAL; MACROPHAGE; MICROGLIA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RETINA; RETINA CELL; RETINA DEGENERATION; RETINAL NEUROEPITHELIAL LAYER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRIATE CORTEX; SUPERIOR COLLICULUS; UPREGULATION; VISUAL CORTEX; VISUAL INFORMATION; VISUAL STIMULATION; ALLOTRANSPLANTATION; ANIMAL; BLINDNESS; CELL SURVIVAL; DEFICIENCY; GENETICS; IMMUNOSUPPRESSIVE TREATMENT; LIGHT; METABOLISM; MUTANT MOUSE STRAIN; MUTATION; PATHOLOGY; RADIATION RESPONSE; STEM CELL TRANSPLANTATION; TIME FACTOR; VERTEBRATE PHOTORECEPTOR CELL;

ANIMALS; BIOMARKERS; BLINDNESS; CELL SURVIVAL; HUMAN EMBRYONIC STEM CELLS; HUMANS; IMMUNOSUPPRESSION; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; LIGHT; MICE; MICE, MUTANT STRAINS; MUTATION; PHOTORECEPTOR CELLS, VERTEBRATE; STEM CELL TRANSPLANTATION; TIME FACTORS; TRANSPLANTATION, HOMOLOGOUS;

EID: 85009728763     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.11.019     Document Type: Article

References (51)

1. Barber, A.C., Hippert, C., Duran, Y., West, E.L., Bainbridge, J.W., Warre-Cornish, K., Luhmann, U.F., Lakowski, J., Sowden, J.C., Ali, R.R., Pearson, R.A., Repair of the degenerate retina by photoreceptor transplantation. Proc. Natl. Acad. Sci. USA 110 (2013), 354–359.
2. Cao, X., Shores, E.W., Hu-Li, J., Anver, M.R., Kelsall, B.L., Russell, S.M., Drago, J., Noguchi, M., Grinberg, A., Bloom, E.T., et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 2 (1995), 223–238.
3. Cao, X., Shen, D., Patel, M.M., Tuo, J., Johnson, T.M., Olsen, T.W., Chan, C.C., Macrophage polarization in the maculae of age-related macular degeneration: a pilot study. Pathol. Int. 61 (2011), 528–535.
4. Chen, M., Xu, H., Parainflammation, chronic inflammation, and age-related macular degeneration. J. Leukoc. Biol. 98 (2015), 713–725.
5. Clarke, L., Ballios, B.G., van der Kooy, D., Generation and clonal isolation of retinal stem cells from human embryonic stem cells. Eur. J. Neurosci. 36 (2012), 1951–1959.
6. Combadière, C., Feumi, C., Raoul, W., Keller, N., Rodéro, M., Pézard, A., Lavalette, S., Houssier, M., Jonet, L., Picard, E., et al. CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J. Clin. Invest. 117 (2007), 2920–2928.
7. Cummings, B.J., Uchida, N., Tamaki, S.J., Salazar, D.L., Hooshmand, M., Summers, R., Gage, F.H., Anderson, A.J., Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc. Natl. Acad. Sci. USA 102 (2005), 14069–14074.
8. DiSanto, J.P., Müller, W., Guy-Grand, D., Fischer, A., Rajewsky, K., Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. Proc. Natl. Acad. Sci. USA 92 (1995), 377–381.
9. Forbes, S.J., Rosenthal, N., Preparing the ground for tissue regeneration: from mechanism to therapy. Nat. Med. 20 (2014), 857–869.
10. Forrester, J.V., Xu, H., Good news-bad news: the Yin and Yang of immune privilege in the eye. Front. Immunol., 3, 2012, 338.
11. Gonzalez-Cordero, A., West, E.L., Pearson, R.A., Duran, Y., Carvalho, L.S., Chu, C.J., Naeem, A., Blackford, S.J., Georgiadis, A., Lakowski, J., et al. Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat. Biotechnol. 31 (2013), 741–747.
12. Gordon, S., Alternative activation of macrophages. Nat. Rev. Immunol. 3 (2003), 23–35.
13. Güler, A.D., Ecker, J.L., Lall, G.S., Haq, S., Altimus, C.M., Liao, H.W., Barnard, A.R., Cahill, H., Badea, T.C., Zhao, H., et al. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453 (2008), 102–105.
14. Gupta, N., Brown, K.E., Milam, A.H., Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp. Eye Res. 76 (2003), 463–471.
15. Hambright, D., Park, K.Y., Brooks, M., McKay, R., Swaroop, A., Nasonkin, I.O., Long-term survival and differentiation of retinal neurons derived from human embryonic stem cell lines in un-immunosuppressed mouse retina. Mol. Vis. 18 (2012), 920–936.
16. Hippert, C., Graca, A.B., Pearson, R.A., Gliosis Can Impede Integration Following Photoreceptor Transplantation into the Diseased Retina. Adv. Exp. Med. Biol. 854 (2016), 579–585.
17. Jiang, L.Q., Jorquera, M., Streilein, J.W., Subretinal space and vitreous cavity as immunologically privileged sites for retinal allografts. Invest. Ophthalmol. Vis. Sci. 34 (1993), 3347–3354.
18. Jiang, L.Q., Jorquera, M., Streilein, J.W., Ishioka, M., Unconventional rejection of neural retinal allografts implanted into the immunologically privileged site of the eye. Transplantation 59 (1995), 1201–1207.
19. Kaewkhaw, R., Kaya, K.D., Brooks, M., Homma, K., Zou, J., Chaitankar, V., Rao, M., Swaroop, A., Transcriptome Dynamics of Developing Photoreceptors in Three-Dimensional Retina Cultures Recapitulates Temporal Sequence of Human Cone and Rod Differentiation Revealing Cell Surface Markers and Gene Networks. Stem Cells 33 (2015), 3504–3518.
20. Lakowski, J., Baron, M., Bainbridge, J., Barber, A.C., Pearson, R.A., Ali, R.R., Sowden, J.C., Cone and rod photoreceptor transplantation in models of the childhood retinopathy Leber congenital amaurosis using flow-sorted Crx-positive donor cells. Hum. Mol. Genet. 19 (2010), 4545–4559.
21. Lall, G.S., Revell, V.L., Momiji, H., Al Enezi, J., Altimus, C.M., Güler, A.D., Aguilar, C., Cameron, M.A., Allender, S., Hankins, M.W., Lucas, R.J., Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron 66 (2010), 417–428.
22. Lamba, D.A., Reh, T.A., Microarray characterization of human embryonic stem cell-derived retinal cultures. Invest. Ophthalmol. Vis. Sci. 52 (2011), 4897–4906.
23. Lamba, D.A., Karl, M.O., Ware, C.B., Reh, T.A., Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 103 (2006), 12769–12774.
24. Lamba, D.A., Gust, J., Reh, T.A., Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell Stem Cell 4 (2009), 73–79.
25. Lamba, D.A., McUsic, A., Hirata, R.K., Wang, P.R., Russell, D., Reh, T.A., Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells. PLoS ONE, 5, 2010, e8763.
26. Lucas, R.J., Hattar, S., Takao, M., Berson, D.M., Foster, R.G., Yau, K.W., Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299 (2003), 245–247.
27. Luo, J., Baranov, P., Patel, S., Ouyang, H., Quach, J., Wu, F., Qiu, A., Luo, H., Hicks, C., Zeng, J., et al. Human retinal progenitor cell transplantation preserves vision. J. Biol. Chem. 289 (2014), 6362–6371.
28. MacLaren, R.E., Pearson, R.A., MacNeil, A., Douglas, R.H., Salt, T.E., Akimoto, M., Swaroop, A., Sowden, J.C., Ali, R.R., Retinal repair by transplantation of photoreceptor precursors. Nature 444 (2006), 203–207.
29. Mellough, C.B., Sernagor, E., Moreno-Gimeno, I., Steel, D.H., Lako, M., Efficient stage-specific differentiation of human pluripotent stem cells toward retinal photoreceptor cells. Stem Cells 30 (2012), 673–686.
30. Meyer, J.S., Howden, S.E., Wallace, K.A., Verhoeven, A.D., Wright, L.S., Capowski, E.E., Pinilla, I., Martin, J.M., Tian, S., Stewart, R., et al. Optic vesicle-like structures derived from human pluripotent stem cells facilitate a customized approach to retinal disease treatment. Stem Cells 29 (2011), 1206–1218.
31. Mills, C.D., M1 and M2 Macrophages: Oracles of Health and Disease. Crit. Rev. Immunol. 32 (2012), 463–488.
32. Nakadate, K., Imamura, K., Watanabe, Y., Effects of monocular deprivation on the spatial pattern of visually induced expression of c-Fos protein. Neuroscience 202 (2012), 17–28.
33. Neves, J., Zhu, J., Sousa-Victor, P., Konjikusic, M., Riley, R., Chew, S., Qi, Y., Jasper, H., Lamba, D.A., Immune modulation by MANF promotes tissue repair and regenerative success in the retina. Science, 353, 2016, aaf3646.
34. Okuno, H., Regulation and function of immediate-early genes in the brain: beyond neuronal activity markers. Neurosci. Res. 69 (2011), 175–186.
35. Panda, S., Provencio, I., Tu, D.C., Pires, S.S., Rollag, M.D., Castrucci, A.M., Pletcher, M.T., Sato, T.K., Wiltshire, T., Andahazy, M., et al. Melanopsin is required for non-image-forming photic responses in blind mice. Science 301 (2003), 525–527.
36. Pearson, R.A., Barber, A.C., Rizzi, M., Hippert, C., Xue, T., West, E.L., Duran, Y., Smith, A.J., Chuang, J.Z., Azam, S.A., et al. Restoration of vision after transplantation of photoreceptors. Nature 485 (2012), 99–103.
37. Pearson, R.A., Hippert, C., Graca, A.B., Barber, A.C., Photoreceptor replacement therapy: challenges presented by the diseased recipient retinal environment. Vis. Neurosci. 31 (2014), 333–344.
38. Pearson, R.A., Gonzalez-Cordero, A., West, E.L., Ribeiro, J.R., Aghaizu, N., Goh, D., Sampson, R.D., Georgiadis, A., Waldron, P.V., Duran, Y., et al. Donor and host photoreceptors engage in material transfer following transplantation of post-mitotic photoreceptor precursors. Nat. Commun., 7, 2016, 13029.
39. Santos-Ferreira, T., Llonch, S., Borsch, O., Postel, K., Haas, J., Ader, M., Retinal transplantation of photoreceptors results in donor-host cytoplasmic exchange. Nat. Commun., 7, 2016, 13028.
40. Seiler, M.J., Aramant, R.B., Jones, M.K., Ferguson, D.L., Bryda, E.C., Keirstead, H.S., A new immunodeficient pigmented retinal degenerate rat strain to study transplantation of human cells without immunosuppression. Graefes Arch. Clin. Exp. Ophthalmol. 252 (2014), 1079–1092.
41. Shirai, H., Mandai, M., Matsushita, K., Kuwahara, A., Yonemura, S., Nakano, T., Assawachananont, J., Kimura, T., Saito, K., Terasaki, H., et al. Transplantation of human embryonic stem cell-derived retinal tissue in two primate models of retinal degeneration. Proc. Natl. Acad. Sci. USA 113 (2016), E81–E90.
42. Singh, M.S., Charbel Issa, P., Butler, R., Martin, C., Lipinski, D.M., Sekaran, S., Barnard, A.R., MacLaren, R.E., Reversal of end-stage retinal degeneration and restoration of visual function by photoreceptor transplantation. Proc. Natl. Acad. Sci. USA 110 (2013), 1101–1106.
43. Tagawa, Y., Kanold, P.O., Majdan, M., Shatz, C.J., Multiple periods of functional ocular dominance plasticity in mouse visual cortex. Nat. Neurosci. 8 (2005), 380–388.
44. Tassoni, A., Gutteridge, A., Barber, A.C., Osborne, A., Martin, K.R., Molecular Mechanisms Mediating Retinal Reactive Gliosis Following Bone Marrow Mesenchymal Stem Cell Transplantation. Stem Cells 33 (2015), 3006–3016.
45. Tucker, B.A., Mullins, R.F., Streb, L.M., Anfinson, K., Eyestone, M.E., Kaalberg, E., Riker, M.J., Drack, A.V., Braun, T.A., Stone, E.M., Patient-specific iPSC-derived photoreceptor precursor cells as a means to investigate retinitis pigmentosa. eLife, 2, 2013, e00824.
46. West, E.L., Pearson, R.A., Barker, S.E., Luhmann, U.F., Maclaren, R.E., Barber, A.C., Duran, Y., Smith, A.J., Sowden, J.C., Ali, R.R., Long-term survival of photoreceptors transplanted into the adult murine neural retina requires immune modulation. Stem Cells 28 (2010), 1997–2007.
47. West, E.L., Gonzalez-Cordero, A., Hippert, C., Osakada, F., Martinez-Barbera, J.P., Pearson, R.A., Sowden, J.C., Takahashi, M., Ali, R.R., Defining the integration capacity of embryonic stem cell-derived photoreceptor precursors. Stem Cells 30 (2012), 1424–1435.
48. Won, J., Shi, L.Y., Hicks, W., Wang, J., Hurd, R., Naggert, J.K., Chang, B., Nishina, P.M., Mouse model resources for vision research. J. Ophthalmol., 2011, 2011, 391384.
49. Yoshida, N., Ikeda, Y., Notomi, S., Ishikawa, K., Murakami, Y., Hisatomi, T., Enaida, H., Ishibashi, T., Laboratory evidence of sustained chronic inflammatory reaction in retinitis pigmentosa. Ophthalmology 120 (2013), e5–e12.
50. Zeng, H.Y., Zhu, X.A., Zhang, C., Yang, L.P., Wu, L.M., Tso, M.O., Identification of sequential events and factors associated with microglial activation, migration, and cytotoxicity in retinal degeneration in rd mice. Invest. Ophthalmol. Vis. Sci. 46 (2005), 2992–2999.
51. Zhong, X., Gutierrez, C., Xue, T., Hampton, C., Vergara, M.N., Cao, L.H., Peters, A., Park, T.S., Zambidis, E.T., Meyer, J.S., et al. Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs. Nat. Commun., 5, 2014, 4047.