A new immunodeficient pigmented retinal degenerate rat strain to study transplantation of human cells without immunosuppression

Graefe's Archive for Clinical and Experimental Ophthalmology

Volumn 252, Issue 7, 2014, Pages 1079-1092

  Seiler, Magdalene J ^a   Aramant, Robert B ^a   Jones, Melissa K ^a,b,c   Ferguson, Dave L ^a   Bryda, Elizabeth C ^d   Keirstead, Hans S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

Human embryonic stem cells; Human neural progenitor cells; Immunodeficiency; Photoreceptor degeneration; Rat strain; Retinal transplantation; Xenografts

Indexed keywords

GENOMIC DNA; RHODOPSIN; BIOLOGICAL MARKER; EYE PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; WHN PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; EXPERIMENTAL RAT; GENE MUTATION; GENOTYPE; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; MALE; MOUSE; NEURAL STEM CELL; NONHUMAN; PHOTORECEPTOR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; RAT STRAIN; RETINA DEGENERATION; RETINAL TRANSPLANTATION; STEM CELL TRANSPLANTATION; TRANSGENE; XENOGRAFT; ANIMAL; CELL SURVIVAL; CONFOCAL MICROSCOPY; DISEASE MODEL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GENOTYPING TECHNIQUE; IMMUNOLOGIC DEFICIENCY SYNDROMES; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; METABOLISM; NUDE RAT; PATHOLOGY; PHYSIOLOGY; RETINAL DEGENERATION; SPRAGUE DAWLEY RAT; TRANSGENIC RAT; TRANSPLANTATION;

ANIMALS; BIOLOGICAL MARKERS; CELL SURVIVAL; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; EYE PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FORKHEAD TRANSCRIPTION FACTORS; GENOTYPING TECHNIQUES; HETEROGRAFTS; HUMANS; IMMUNE TOLERANCE; IMMUNOLOGIC DEFICIENCY SYNDROMES; IMMUNOSUPPRESSION; MALE; MICROSCOPY, CONFOCAL; RATS; RATS, NUDE; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RETINAL DEGENERATION; STEM CELL TRANSPLANTATION;

EID: 84904349972     PISSN: 0721832X     EISSN: 1435702X     Source Type: Journal    
DOI: 10.1007/s00417-014-2638-y     Document Type: Article

References (61)

1. Nussenblatt RB, Liu B, Li Z (2009) Age-related macular degeneration: an immunologically driven disease. Curr Opin Investig Drugs 10:434-442
2. Sahel J, Bonnel S, Mrejen S, Paques M (2010) Retinitis pigmentosa and other dystrophies. Dev Ophthalmol 47:160-167. doi:10.1159/000320079
3. Huang Y, Enzmann V, Ildstad ST (2011) Stem cell-based therapeutic applications in retinal degenerative diseases. Stem Cell Rev 7:434-445. doi:10.1007/s12015-010-9192-8
4. Kokotas H, Grigoriadou M, Petersen MB (2011) Age-related macular degeneration: genetic and clinical findings. Clin Chem Lab Med 49:601-616. doi:10.1515/CCLM.2011.091
5. Trifunovic D, Sahaboglu A, Kaur J, Mencl S, Zrenner E, Ueffing M, Arango-Gonzalez B, Paquet-Durand F (2012) Neuroprotective strategies for the treatment of inherited photoreceptor degeneration. Curr Mol Med 12:598-612
6. Sin HP, Liu DT, Lam DS (2012) Lifestyle modification, nutritional and vitamins supplements for age-relatedmacular degeneration. Acta Ophthalmol. doi:10.1111/j.1755-3768.2011.02357.x
7. Wen R, Tao W, Li Y, Sieving PA (2012) CNTF and retina. Prog Retin Eye Res 31:136-151. doi:10.1016/j.preteyeres.2011.11.005
8. Thanos C, Emerich D (2005) Delivery of neurotrophic factors and therapeutic proteins for retinal diseases. Expert Opin Biol Ther 5:1443-1452. doi:10.1517/14712598.5.11.1443 (Pubitemid 41579429)
9. LaVail MM (2005) Survival factors for treatment of retinal degenerative disorders: preclinical gains and issues for translation into clinical studies. Retina 25:S25-S26
10. Lund R (2008) Cell-based therapies to limit photoreceptor degeneration. Arch Soc Esp Oftalmol 83:457-464
11. Schwartz SD, Hubschman JP, Heilwell G, Franco-Cardenas V, Pan CK, Ostrick RM, Mickunas E, Gay R, Klimanskaya I, Lanza R (2012) Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 379:713-720. doi:10.1016/S0140-6736(12)60028-2
12. Klassen HJ, Ng TF, Kurimoto Y, Kirov I, Shatos M, Coffey P, Young MJ (2004) Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Invest Ophthalmol Vis Sci 45:4167-4173. doi:10.1167/iovs.04-0511 (Pubitemid 39411176)
13. Singh MS, Charbel Issa P, Butler R, Martin C, Lipinski DM, Sekaran S, Barnard AR, MacLaren RE (2013) Reversal of end-stage retinal degeneration and restoration of visual function by photoreceptor transplantation. Proc Natl Acad Sci U S A 110:1101-1106. doi:10.1073/pnas.1119416110
14. 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. doi:10.1016/j.stem.2008.10.015
15. 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 (Pubitemid 44722060)
16. Mansergh FC, Vawda R, Millington-Ward S, Kenna PF, Haas J, Gallagher C, Wilson JH, Humphries P, Ader M, Farrar GJ (2010) Loss of photoreceptor potential from retinal progenitor cell cultures, despite improvements in survival. Exp Eye Res 91:500-512. doi:10.1016/j.exer.2010.07.003
17. Aramant RB, Seiler MJ (2004) Progress in retinal sheet transplantation. Prog Retin Eye Res 23:475-494 (Pubitemid 39078358)
18. Seiler MJ, Aramant RB, Keirstead HS (2008) Retinal transplants: hope to preserve and restore vision? Opt Photonics News 19:37-47
19. Seiler MJ, Aramant RB (2012) Cell replacement and visual restoration by retinal sheet transplants. Prog Retin Eye Res 31:661-687. doi:10.1016/j. preteyeres.2012.06.003
20. Radtke ND, Aramant RB, Petry HM, Green PT, Pidwell DJ, Seiler MJ (2008) Vision improvement in retinal degeneration patients by implantation of retina together with retinal pigment epithelium. Am J Ophthalmol 146:172-182. doi:10.1016/j.ajo.2008.04.009
21. Meyer JS, Shearer RL, Capowski EE, Wright LS, Wallace KA, McMillan EL, Zhang SC, Gamm DM (2009) Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proc Natl Acad Sci U S A 106:16698-16703. doi:10.1073/pnas.0905245106
22. Yue F, Johkura K, Shirasawa S, Yokoyama T, Inoue Y, Tomotsune D, Sasaki K (2010) Differentiation of primate ES cells into retinal cells induced by ES cell-derived pigmented cells. Biochem Biophys Res Commun 394:877-883. doi:10.1016/j.bbrc.2010.03.008
23. 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. doi:10.1371/journal. pone.0008763
24. Tucker BA, Park IH, Qi SD, Klassen HJ, Jiang C, Yao J, Redenti S, Daley GQ, Young MJ (2011) Transplantation of adult mouse iPS cell-derived photoreceptor precursors restores retinal structure and function in degenerative mice. PLoS One 6:e18992. doi:10.1371/journal.pone.0018992
25. Meyer JS, Howden SE, Wallace KA, Verhoeven AD, Wright LS, Capowski EE, Pinilla I, Martin JM, Tian S, Stewart R, Pattnaik B, Thomson JA, Gamm DM (2011) Optic vesicle-like structures derived from human pluripotent stem cells facilitate a customized approach to retinal disease treatment. Stem Cells 29:1206-1218. doi:10.1002/stem.674
26. Parameswaran S, Balasubramanian S, Babai N, Qiu F, Eudy JD, Thoreson WB, Ahmad I (2010) Induced pluripotent stem cells generate both retinal ganglion cells and photoreceptors: therapeutic implications in degenerative changes in glaucoma and age-related macular degeneration. Stem Cells 28:695-703. doi:10.1002/stem.320
27. Hambright D, Park KY, Brooks M, McKay R, Swaroop A, Nasonkin IO (2012) Long-term survival and differentiation of retinal neurons derived from human embryonic stem cell lines in unimmunosuppressed mouse retina. Mol Vis 18:920-936
28. Nakano T, Ando S, Takata N, Kawada M, Muguruma K, Sekiguchi K, Saito K, Yonemura S, Eiraku M, Sasai Y (2012) Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10:771-785. doi:10.1016/j.stem.2012.05.009
29. Steinberg RH, Flannery JG, Naash M, Oh P, Matthes MT, Yasumura D, Lau-Villacorta C, Chen J, LaVail MM (1996) Transgenic rat models of inherited retinal degeneration caused by mutant opsin genes [ARVO abstract]. Invest Ophthalmol Vis Sci 37:S698 (Pubitemid 126824667)
30. Pennesi ME, Nishikawa S, Matthes MT, Yasumura D, LaVail MM (2008) The relationship of photoreceptor degeneration to retinal vascular development and loss in mutant rhodopsin transgenic and RCS rats. Exp Eye Res 87:561-570. doi:10.1016/j.exer.2008.09.004
31. Martinez-Navarrete G, Seiler MJ, Aramant RB, Fernandez-Sanchez L, Pinilla I, Cuenca N (2011) Retinal degeneration in two lines of transgenic S334ter rats. Exp Eye Res 92:227-237. doi:10.1016/j.exer.2010.12.001
32. Segre JA, Nemhauser JL, Taylor BA, Nadeau JH, Lander ES (1995) Positional cloning of the nude locus: genetic, physical, and transcription maps of the region andmutations in the mouse and rat. Genomics 28:549-559. doi:10.1006/geno.1995.1187
33. Hirasawa T, Yamashita H, Makino S (1998) Genetic typing of the mouse and rat nude mutations by PCR and restriction enzyme analysis. Exp Anim 47:63-67 (Pubitemid 128443117)
34. Aramant RB, Seiler MJ (1994) Human embryonic retinal cell transplants in athymic immunodeficient rat hosts. Cell Transplant 3:461-474 (Pubitemid 24372206)
35. Guest JD, Rao A, Olson L, Bunge MB, Bunge RP (1997) The ability of human Schwann cell grafts to promote regeneration in the transected nude rat spinal cord. Exp Neurol 148:502-522. doi:10.1006/exnr.1997.6693 (Pubitemid 28068845)
36. Aramant RB, Seiler MJ (2002) Transplanted sheets of human retina and retinal pigment epithelium develop normally in nude rats. Exp Eye Res 75:115-125
37. Nasonkin I, Mahairaki V, Xu L, Hatfield G, Cummings BJ, Eberhart C, Ryugo DK, Maric D, Bar E, Koliatsos VE (2009) Long-term, stable differentiation of human embryonic stem cell-derived neural precursors grafted into the adult mammalian neostriatum. Stem Cells 27:2414-2426. doi:10.1002/stem.177
38. Liang SC, Lin SZ, Yu JF, Wu SF, Wang SD, Liu JC (1997) F344-rnu/rnu athymic rats: breeding performance and acceptance of subcutaneous and intracranial xenografts at different ages. Lab Anim Sci 47:549-553
39. Nistor G, Seiler MJ, Yan F, Ferguson D, Keirstead HS (2010) Three-dimensional early retinal progenitor 3D tissue constructs derived from human embryonic stem cells. J Neurosci Methods 190:63-70. doi:10.1016/j. jneumeth.2010.04.025
40. Aramant RB, Seiler MJ (2002) Retinal transplantation - advantages of intact fetal sheets. Prog Retin Eye Res 21:57-73 (Pubitemid 34242707)
41. 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 (Pubitemid 44298636)
42. Vugler AA (2010) Progress toward the maintenance and repair of degenerating retinal circuitry. Retina 30:983-1001. doi:10.1097/IAE. 0b013e3181e2a680
43. Clarke L, Ballios BG, van der Kooy D (2012) Generation and clonal isolation of retinal stem cells from human embryonic stemcells. Eur J Neurosci 36:1951-1959. doi:10.1111/j.1460-9568.2012.08123.x
44. Thliveris JA, Yatscoff RW, Lukowski MP, Copeland KR (1991) Cyclosporine nephrotoxicity-experimental models. Clin Biochem 24:93-95
45. Cibulskyte D, Kaalund H, Pedersen M, Horlyck A, Marcussen N, Hansen HE, Madsen M, Mortensen J (2005) Chronic cyclosporine nephrotoxicity: a pig model. Transplant Proc 37:3298-3301. doi:10.1016/j.transproceed.2005.09.004 (Pubitemid 41659871)
46. Granholm AC, Eriksdotter-Nilsson M, Stromberg I, Stieg P, Seiger A, Bygdeman M, Geffard M, Oertel W, Dahl D, Olson L et al (1989) Morphological and electrophysiological studies of human hippocampal transplants in the anterior eye chamber of athymic nude rats. Exp Neurol 104:162-171 (Pubitemid 19122844)
47. Hall M, Wang Y, Granholm AC, Stevens JO, Young D, Hoffer BJ (1992) Comparison of fetal rabbit brain xenografts to three different strains of athymic nude rats: electrophysiological and immunohistochemical studies of intraocular grafts. Cell Transplant 1:71-82
48. Kim M, Park IY, Lim J, Kim Y, Han KT, Chung WH, Han K (2006) Antitumor and normal cell protective effect of PKC412 in the athymic mouse model of ovarian cancer. Ann Clin Lab Sci 36:455-460 (Pubitemid 44786694)
49. Hurelbrink CB, Barker RA (2005) Migration of cells from primary transplants of allo- and xenografted foetal striatal tissue in the adult rat brain. Eur J Neurosci 21:1503-1510. doi:10.1111/j.1460-9568.2005.03963.x (Pubitemid 40646596)
50. Anderson AJ, Haus DL, Hooshmand MJ, Perez H, Sontag CJ, Cummings BJ (2011) Achieving stable human stem cell engraftment and survival in the CNS: is the future of regenerative medicine immunodeficient? Regen Med 6:367-406. doi:10.2217/rme.11.22
51. Phillips MJ, Wallace KA, Dickerson SJ, Miller MJ, Verhoeven A, Martin JM, Wright L, Shen W, Capowski EE, Percin EF, Perez ET, Zhong X, Canto-Soler MV, Gamm DM (2012) Blood-derived human iPS cells generate optic vesicle-like structures with the capacity to form retinal laminae and develop synapses. Invest Ophthalmol Vis Sci 53:2007-2019. doi:10.1167/iovs.11-9313
52. Seiler MJ, Aramant RB, Thomas BB, Peng Q, Sadda SR, Keirstead HS (2010) Visual restoration and transplant connectivity in degenerate rats implanted with retinal progenitor sheets. Eur J Neurosci 31:508-520. doi:10.1111/j.1460-9568. 2010.07085.x
53. Yang PB, Seiler MJ, Aramant RB, Yan F, Mahoney MJ, Kitzes LM, Keirstead HS (2010) Trophic factors GDNF and BDNF improve function of retinal sheet transplants. Exp Eye Res 91:727-738. doi:10.1016/j.exer.2010.08.022
54. Niederkorn JY (2006) See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat Immunol 7:354-359. doi:10.1038/ni1328
55. Lund RD, Ono SJ, Keegan DJ, Lawrence JM (2003) Retinal transplantation: progress and problems in clinical application. J Leukoc Biol 74:151-160 (Pubitemid 38040410)
56. Banerjee R, Lund RD, Radel JD (1993) Anatomical and functional consequences of induced rejection of intracranial retinal transplants. Neuroscience 56:939-953 (Pubitemid 23308649)
57. Donoso LA, Merryman CF, Edelberg KE, Naids R, Kalsow C (1985) S-Antigen in the developing retina and pineal gland: a monoclonal antibody study. Invest Ophthalmol Vis Sci 26:561-567 (Pubitemid 15059020)
58. Saari JC, Bunt-Milam AH, Bredberg DL, Garwin GG (1984) Properties and immunocytochemical localization of three retinoid-binding proteins from bovine retina. Vis Res 24:1595-1603 (Pubitemid 15181716)
59. Mears AJ, Kondo M, Swain PK, Takada Y, Bush RA, Saunders TL, Sieving PA, Swaroop A (2001) Nrl is required for rod photoreceptor development. Nat Genet 29:447-452. doi:10.1038/ng774 (Pubitemid 34326696)
60. Dizhoor AM, Ray S, Kumar S, Niemi G, Spencer M, Brolley D, Walsh KA, Philipov PP, Hurley JB, Stryer L (1991) Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase. Science 251:915-918 (Pubitemid 21926182)
61. Molday RS, MacKenzie D (1983) Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry 22:653-660