Optogenetic control of neural differentiation in Opto-mGluR6 engineered retinal pigment epithelial cell line and mesenchymal stem cells.
mesenchymal stem cells
optogenetic stimulation
retinal degenerative disorders
retinal differentiation
retinal pigment epithelial cells
Journal
Journal of cellular biochemistry
ISSN: 1097-4644
Titre abrégé: J Cell Biochem
Pays: United States
ID NLM: 8205768
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
26
02
2021
received:
30
12
2020
accepted:
01
03
2021
pubmed:
14
4
2021
medline:
3
9
2021
entrez:
13
4
2021
Statut:
ppublish
Résumé
In retinal degenerative disorders, when neural retinal cells are damaged, cell transplantation is one of the most promising therapeutic approaches. Optogenetic technology plays an essential role in the neural differentiation of stem cells via membrane depolarization. This study explored the efficacy of blue light stimulation in neuroretinal differentiation of Opto-mGluR6-engineered mouse retinal pigment epithelium (mRPE) and bone marrow mesenchymal stem cells (BMSCs). mRPE and BMSCs were selected for optogenetic study due to their capability to differentiate into retinal-specific neurons. BMSCs were isolated and phenotypically characterized by the expression of mesenchymal stem cell-specific markers, CD44 (99%) and CD105 (98.8%). mRPE culture identity was confirmed by expression of RPE-specific marker, RPE65, and epithelial cell marker, ZO-1. mRPE cells and BMSCs were transduced with AAV-MCS-IRES-EGFP-Opto-mGluR6 viral vector and stimulated for 5 days with blue light (470 nm). RNA and protein expression of Opto-mGluR6 were verified. Optogenetic stimulation-induced elevated intracellular Ca
Substances chimiques
Receptors, Metabotropic Glutamate
0
metabotropic glutamate receptor 6
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
851-869Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Veleri S, Lazar CH, Chang B, Sieving PA, Banin E, Swaroop A. Biology and therapy of inherited retinal degenerative disease: insights from mouse models. Dis Models & Mech. 2015;8(2):109-129. https://doi.org/10.1242/dmm.017913
Zarbin M. Cell-based therapy for degenerative retinal disease. Trends Mol Med. 2016;22(2):115-134.
Lee S, Chang H, Kim S. Incorporation and differentiation of human adipose tissue-derived stem cells in injured athymic nude mouse retina. Invest Ophthalmol Visual Sci. 2009;50(13):5133.
Benowitz LI, Yin Y. Optic nerve regeneration. Arch Ophthalmol . 2010;128(8):1059-1064. https://doi.org/10.1001/archophthalmol.2010.152
Gorecka J, Kostiuk V, Fereydooni A, et al. The potential and limitations of induced pluripotent stem cells to achieve wound healing. Stem Cell Res Ther. 2019;10(1):87. https://doi.org/10.1186/s13287-019-1185-1
Tang Z, Zhang Y, Wang Y, et al. Progress of stem/progenitor cell-based therapy for retinal degeneration. J Transl Med. 2017;15(1):99. https://doi.org/10.1186/s12967-017-1183-y
Dutt K, Cao Y. Engineering retina from human retinal progenitors (cell lines). Tissue Eng Part A. 2009;15(6):1401-1413. https://doi.org/10.1089/ten.tea.2007.0358
Falkner-Radler CI, Krebs I, Glittenberg C, et al. Human retinal pigment epithelium (RPE) transplantation: outcome after autologous RPE-choroid sheet and RPE cell-suspension in a randomised clinical study. Br J Ophthalmol. 2010;95(3):370-375.
Falkner-Radler CI, Krebs I, Glittenberg C, et al. Human retinal pigment epithelium (RPE) transplantation: outcome after autologous RPE-choroid sheet and RPE cell-suspension in a randomised clinical study. Br J Ophthalmol. 2010;2009:176305.
Mathivanan I, Trepp C, Brunold C, Baerlocher G, Enzmann V. Retinal differentiation of human bone marrow-derived stem cells by co-culture with retinal pigment epithelium in vitro. Exp Cell Res. 2015;333(1):11-20. https://doi.org/10.1016/j.yexcr.2015.02.001
Qiu G, Seiler MJ, Mui C, et al. Photoreceptor differentiation and integration of retinal progenitor cells transplanted into transgenic rats. Exp Eye Res. 2005;80(4):515-525.
Schwartz SD, Regillo CD, Lam BL, et al. Human embryonic stem cell-derived retinal pigment epithelium in patients with age-related macular degeneration and Stargardt's macular dystrophy: follow-up of two open-label phase 1/2 studies. The Lancet. 2014;385(9968):509-516.
Wang S-Z, Ma W, Yan R-T, Mao W. Generating retinal neurons by reprogramming retinal pigment epithelial cells. Expert Opin Biol Ther. 2010;10(8):1227-1239. https://doi.org/10.1517/14712598.2010.495218
Zhang W, Wang Y, Kong J, Dong M, Duan H, Chen S. Therapeutic efficacy of neural stem cells originating from umbilical cord-derived mesenchymal stem cells in diabetic retinopathy. Sci Rep. 2017;7(1):408. https://doi.org/10.1038/s41598-017-00298-2
Simó R, Villarroel M, Corraliza L, Hernández C, Garcia-Ramírez M. The retinal pigment epithelium: something more than a constituent of the blood-retinal barrier-implications for the pathogenesis of diabetic retinopathy. BioMed Res Int. 2010(2010):190724.
Luz-Madrigal A, Grajales-Esquivel E, McCorkle A, et al. Reprogramming of the chick retinal pigmented epithelium after retinal injury. BMC Biol. 2014;12:28. https://doi.org/10.1186/1741-7007-12-28
Ma W, Yan R-T, Li X, Wang S-Z. Reprogramming retinal pigment epithelium to differentiate toward retinal neurons with Sox2. Stem Cells (Dayton, Ohio). 2009;27(6):1376-1387. https://doi.org/10.1002/stem.48
Han Y, Li X, Zhang Y, Han Y, Chang F, Ding J. Mesenchymal stem cells for regenerative medicine. Cells. 2019;8(8):886.
Harrell CR, Fellabaum C, Arsenijevic A, Markovic BS, Djonov V, Volarevic V. Therapeutic potential of mesenchymal stem cells and their secretome in the treatment of glaucoma. Stem Cells Int. 2019;2019:1-11.
Holan V, Hermankova B, Kossl J. Perspectives of stem cell-based therapy for age-related retinal degenerative diseases. Cell Transplant. 2017;26(9):1538-1541. https://doi.org/10.1177/0963689717721227
Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, De Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature. 2007;450(7168):420-424.
Chow, BY, Han X, Dobry AS, et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature. 2010;463(7277):98-102.
Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science. 2009;324(5925):354-359.
Zhao, S, Cunha C, Zhang F, et al. Improved expression of halorhodopsin for light-induced silencing of neuronal activity. Brain Cell Biol. 2008;36(1-4):141-154.
Mirzapour Delavar H, Karamzadeh A, Pahlavanneshan S. Shining light on the sprout of life: optogenetics applications in stem cell research and therapy. J Membr Biol. 2016;249(3):215-220. https://doi.org/10.1007/s00232-016-9883-4
Sekharan S, Wei JN, Batista VS. The active site of melanopsin: the biological clock photoreceptor. J Am Chem Soc. 2012;134(48):19536-19539. https://doi.org/10.1021/ja308763b
Tian L, Kammermeier PJ. G protein coupling profile of mGluR6 and expression of Gα proteins in retinal ON bipolar cells. Visual Neurosci. 2006;23(6):909-916.
van Wyk M, Pielecka-Fortuna J, Löwel S, Kleinlogel S. Restoring the ON switch in blind retinas: opto-mGluR6, a next-generation, cell-tailored optogenetic tool. PLOS Biol. 2015;13(5):e1002143. https://doi.org/10.1371/journal.pbio.1002143
Martemyanov KA. G protein signaling in the retina and beyond: the Cogan lecture. Invest Ophthalmol Visual Sci. 2014;55(12):8201-8207. https://doi.org/10.1167/iovs.14-15928
Huang S, Xu L, Sun Y, Wu T, Wang K, Li G. An improved protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. J Orthop Transl. 2015;3(1):26-33.
Ranaei Pirmardan E, Soheili Z-S, Samiei S, et al. Characterization of a spontaneously generated murine retinal pigmented epithelium cell line; a model for in vitro experiments. Exp Cell Res. 2016;347(2):332-338. https://doi.org/10.1016/j.yexcr.2016.08.015
Rezanejad H, Soheili Z-S, Haddad F, et al. In vitro differentiation of adipose-tissue-derived mesenchymal stem cells into neural retinal cells through expression of human PAX6 (5a) gene. Cell Tissue Res. 2014;356(1):65-75. https://doi.org/10.1007/s00441-014-1795-y
McClure C, Cole KLH, Wulff P, Klugmann M, Murray AJ. Production and titering of recombinant adeno-associated viral vectors. J Vis Exp. 2011;57:e3348. https://doi.org/10.3791/3348
McMahon JM, Conroy S, Lyons M, et al. Gene transfer into rat mesenchymal stem cells: a comparative study of viral and nonviral vectors. Stem Cells Dev. 2006;15(1):87-96. https://doi.org/10.1089/scd.2006.15.87
Xiang M. Intrinsic control of mammalian retinogenesis. Cell Mol Life Sci. 2013;70(14):2519-2532. https://doi.org/10.1007/s00018-012-1183-2
Ge J, Sun X, Jiang R, et al. E13.5 retinal precursor cells induce bone marrow mesenchymal stem cells towards retinal ganglion-like cells. Invest Ophthalmol Visual Sci. 2008;49(13):5474.
Zhang J, Shan Q, Ma P, et al. Differentiation potential of bone marrow mesenchymal stem cells into retina in normal and laser-injured rat eye. Sci China, Ser C: Life Sci. 2004;47(3):241-250.
Tomita M, Adachi Y, Yamada H, et al. Bone marrow-derived stem cells can differentiate into retinal cells in injured rat retina. Stem Cells. 2002;20(4):279-283.
Tomita M, Adachi Y, Yamada H, et al. Bone marrow-derived stem cells can differentiate into retinal neural cells in injured rat retina and in pigmentary retinal degeneration rats. Invest Ophthalmol Visual Sci. 2003;44(13):1688.
Kuroda S, Shichinohe H, Houkin K, Iwasaki Y. Autologous bone marrow stromal cell transplantation for central nervous system disorders-recent progress and perspective for clinical application. J Stem Cells Regen Med. 2011;7(1):2-13. https://doi.org/10.46582/jsrm.0701002
Ryu J, Vincent PFY, Ziogas NK, et al. Optogenetically transduced human ES cell-derived neural progenitors and their neuronal progenies: phenotypic characterization and responses to optical stimulation. PLOS One. 2019;14(11):e0224846. https://doi.org/10.1371/journal.pone.0224846
Stroh A, Tsai HC, Wang LP, et al. Tracking stem cell differentiation in the setting of automated optogenetic stimulation. Stem Cells. 2011;29(1):78-88.
Wang S, Du L, Peng G-H. Optogenetic stimulation inhibits the self-renewal of mouse embryonic stem cells. Cell Biosci. 2019b;9(1):1-13.
Köhidi T, Jády AG, Markó K, et al. Differentiation-dependent motility-responses of developing neural progenitors to optogenetic stimulation. Front Cell Neurosci. 2017;11:401.
Jung K, Park JH, Kim S-Y, Jeon NL, Cho S-R, Hyung S. Optogenetic stimulation promotes Schwann cell proliferation, differentiation, and myelination in vitro. Sci Rep. 2019;9(1):3487. https://doi.org/10.1038/s41598-019-40173-w
Ono K, Suzuki H, Yamamoto R, Sahashi H, Takido Y, Sawada M. Optogenetic control of cell differentiation in channelrhodopsin-2-expressing OS3, a bipotential glial progenitor cell line. Neurochem Int. 2017;104:49-63. https://doi.org/10.1016/j.neuint.2016.12.022
Wang SJ, Weng CH, Xu HW, Zhao CJ, Yin ZQ. Effect of optogenetic stimulus on the proliferation and cell cycle progression of neural stem cells. J Membr Biol. 2014;247(6):493-500.
Wang S, Du L, Peng G-H. Optogenetic stimulation inhibits the self-renewal of mouse embryonic stem cells. Cell Biosci. 2019;9(1):73. https://doi.org/10.1186/s13578-019-0335-6
Elliott J, Jolicoeur C, Ramamurthy V, Cayouette M. Ikaros confers early temporal competence to mouse retinal progenitor cells. Neuron. 2008;60(1):26-39. https://doi.org/10.1016/j.neuron.2008.08.008
Rumelt S. Glaucoma: Basic and Clinical Concepts, 2011. BoD-Books on Demand.
de Melo J, Du G, Fonseca M, et al. Dlx1 and Dlx2 function is necessary for terminal differentiation and survival of late-born retinal ganglion cells in the developing mouse retina. Development. 2005;132(2):311-322. https://doi.org/10.1242/dev.01560
Mo Z, Li S, Yang X, Xiang M. Role of the Barhl2 homeobox gene in the specification of glycinergic amacrine cells. Development. 2004;131(7):1607-1618. https://doi.org/10.1242/dev.01071
Xiang M, Jiang H, Jin K, Qiu F. Molecular control of retinal ganglion cell specification and differentiation. Glaucoma Basic Clin Concepts. 2011:65.
Mao C-A, Kiyama T, Pan P, Furuta Y, Hadjantonakis A-K, Klein WH. Eomesodermin, a target gene of Pou4f2, is required for retinal ganglion cell and optic nerve development in the mouse. Development. 2008;135(2):271-280. https://doi.org/10.1242/dev.009688
de Melo J, Peng G-H, Chen S, Blackshaw S. The Spalt family transcription factor Sall3 regulates the development of cone photoreceptors and retinal horizontal interneurons. Development. 2011;138(11):2325-2336. https://doi.org/10.1242/dev.061846
Jin K, Jiang H, Mo Z, Xiang M. Early B-cell factors are required for specifying multiple retinal cell types and subtypes from postmitotic precursors. J Neurosci. 2010;30(36):11902-11916. https://doi.org/10.1523/JNEUROSCI.2187-10.2010
Jusuf PR, Albadri S, Paolini A, et al. Biasing amacrine subtypes in the Atoh7 lineage through expression of Barhl2. J Neurosci. 2012;32(40):13929-13944. https://doi.org/10.1523/JNEUROSCI.2073-12.2012
Ding Q, Chen H, Xie X, Libby RT, Tian N, Gan L. BARHL2 differentially regulates the development of retinal amacrine and ganglion neurons. J Neurosci. 2009;29(13):3992-4003. https://doi.org/10.1523/JNEUROSCI.5237-08.2009
Balasubramanian R, Gan L. Development of retinal amacrine cells and their dendritic stratification. Current Ophthalmol Rep. 2014;2(3):100-106. https://doi.org/10.1007/s40135-014-0048-2
Vaney DI. Chapter 2 The mosaic of amacrine cells in the mammalian retina. Prog Retin Res. 1990;9:49-100. https://doi.org/10.1016/0278-4327(90)90004-2
Li S, Mo Z, Yang X, Price SM, Shen MM, Xiang M. Foxn4 controls the genesis of amacrine and horizontal cells by retinal progenitors. Neuron. 2004;43(6):795-807. https://doi.org/10.1016/j.neuron.2004.08.041
Nakhai H, Sel S, Favor J, et al. Ptf1a is essential for the differentiation of GABAergic and glycinergic amacrine cells and horizontal cells in the mouse retina. Development. 2007;134(6):1151-1160. https://doi.org/10.1242/dev.02781
Yan R-T, Wang S-Z. Requirement of NeuroD for photoreceptor formation in the chick retina. Invest Ophthalmol Visual Sci. 2004;45(1):48-58. https://doi.org/10.1167/iovs.03-0774
Cherry TJ, Wang S, Bormuth I, Schwab M, Olson J, Cepko CL. NeuroD factors regulate cell fate and neurite stratification in the developing retina. J Neurosci. 2011;31(20):7365-7379. https://doi.org/10.1523/JNEUROSCI.2555-10.2011
Kay JN, Voinescu PE, Chu MW, Sanes JR. Neurod6 expression defines new retinal amacrine cell subtypes and regulates their fate. Nat Neurosci. 2011;14(8):965-972. https://doi.org/10.1038/nn.2859
Koike C, Nishida A, Ueno S, et al. Functional roles of Otx2 transcription factor in postnatal mouse retinal development. Mol Cell Biol. 2007;27(23):8318-8329. https://doi.org/10.1128/MCB.01209-07
Nishida A, Furukawa A, Koike C, et al. Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat Neurosci. 2003;6(12):1255-1263. https://doi.org/10.1038/nn1155
Chen, CMA, Cepko CL. The chicken RaxL gene plays a role in the initiation of photoreceptor differentiation. Development. 2002;129(23):5363-5375. https://doi.org/10.1242/dev.00114
Katoh K, Omori Y, Onishi A, Sato S, Kondo M, Furukawa T. Blimp1 suppresses Chx10 expression in differentiating retinal photoreceptor precursors to ensure proper photoreceptor development. J Neurosci. 2010;30(19):6515-6526. https://doi.org/10.1523/JNEUROSCI.0771-10.2010
Akagi T, Akita J, Haruta M, et al. Iris-derived cells from adult rodents and primates adopt photoreceptor-specific phenotypes. Invest Ophthalmol Visual Sci. 2005;46(9):3411-3419. https://doi.org/10.1167/iovs.04-1112
Chen J, Rattner A, Nathans J. The rod photoreceptor-specific nuclear receptor Nr2e3 represses transcription of multiple cone-specific genes. J Neurosci. 2005;25(1):118-129. https://doi.org/10.1523/JNEUROSCI.3571-04.2005
Jia L, Oh ECT, Ng L, et al. Retinoid-related orphan nuclear receptor RORbeta is an early-acting factor in rod photoreceptor development. Proc Natl Acad Sci U S A. 2009;106(41):17534-17539. https://doi.org/10.1073/pnas.0902425106
Liu H, Etter P, Hayes S, et al. NeuroD1 regulates expression of thyroid hormone receptor β2 and cone opsins in the developing mouse retina. J Neurosci. 2008;28(3):749-756. https://doi.org/10.1523/jneurosci.4832-07.2008
Oh ECT, Cheng H, Hao H, Jia L, Khan NW, Swaroop A. Rod differentiation factor NRL activates the expression of nuclear receptor NR2E3 to suppress the development of cone photoreceptors. Brain Res. 2008;1236:16-29. https://doi.org/10.1016/j.brainres.2008.01.028
Onishi A, Peng G-H, Chen S, Blackshaw S. Pias3-dependent SUMOylation controls mammalian cone photoreceptor differentiation. Nat Neurosci. 2010;13(9):1059-1065. https://doi.org/10.1038/nn.2618
Satoh S, Tang K, Iida A, et al. The spatial patterning of mouse cone opsin expression is regulated by bone morphogenetic protein signaling through downstream effector COUP-TF nuclear receptors. J Neurosci. 2009;29(40):12401-12411.
Srinivas M, Ng L, Liu H, Jia L, Forrest D. Activation of the blue opsin gene in cone photoreceptor development by retinoid-related orphan receptor β. Mol Endocrinol. 2006;20(8):1728-1741. https://doi.org/10.1210/me.2005-0505
Roberts MR, Hendrickson A, McGuire CR, Reh TA. Retinoid X receptor γ is necessary to establish the S-opsin gradient in cone photoreceptors of the developing mouse retina. Invest Ophthalmol Visual Sci. 2005;46(8):2897-2904.
Li Y, Hao H, Swerdel MR, et al. Top2b is involved in the formation of outer segment and synapse during late-stage photoreceptor differentiation by controlling key genes of photoreceptor transcriptional regulatory network. J Neurosci Res. 2017;95(10):1951-1964. https://doi.org/10.1002/jnr.24037
Nelson BR, Hartman BH, Ray CA, Hayashi T, Bermingham-McDonogh O, Reh TA. Acheate-scute like 1 (Ascl1) is required for normal delta-like (Dll) gene expression and notch signaling during retinal development. Dev Dyn. 2009;238(9):2163-2178. https://doi.org/10.1002/dvdy.21848
Pollak J, Wilken MS, Ueki Y, et al. ASCL1 reprograms mouse Muller glia into neurogenic retinal progenitors. Development. 2013;140(12):2619-2631. https://doi.org/10.1242/dev.091355
Furukawa T, Mukherjee S, Bao Z-Z, Morrow EM, Cepko CL. rax, Hes1, and notch1 promote the formation of Müller Glia by postnatal retinal progenitor cells. Neuron. 2000;26(2):383-394. https://doi.org/10.1016/S0896-6273(00)81171-X
Muto A, Iida A, Satoh S, Watanabe S. The group E Sox genes Sox8 and Sox9 are regulated by Notch signaling and are required for Müller glial cell development in mouse retina. Exp Eye Res. 2009;89(4):549-558. https://doi.org/10.1016/j.exer.2009.05.006
Hojo M, Ohtsuka T, Hashimoto N, Gradwohl G, Guillemot F, Kageyama R. Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development. 2000;127(12):2515.
Azuma N, Tadokoro K, Asaka A, et al. Transdifferentiation of the retinal pigment epithelia to the neural retina by transfer of the Pax6 transcriptional factor. Hum Mol Gen. 2005;14(8):1059-1068. https://doi.org/10.1093/hmg/ddi098
Kicic A, Shen W-Y, Wilson AS, Constable IJ, Robertson T, Rakoczy PE. Differentiation of marrow stromal cells into photoreceptors in the rat eye. J Neurosci. 2003;23(21):7742-7749. https://doi.org/10.1523/JNEUROSCI.23-21-07742.2003
Tomita M, Adachi Y, Yamada H, et al. Bone marrow-derived stem cells can differentiate into retinal cells in injured rat retina. Stem Cells. 2002a;20(4):279-283. https://doi.org/10.1634/stemcells.20-4-279
Qu L, Gao L, Xu H, et al. Combined transplantation of human mesenchymal stem cells and human retinal progenitor cells into the subretinal space of RCS rats. Sci Rep. 2017;7(1):199. https://doi.org/10.1038/s41598-017-00241-5
Otify DY, Youssef E, Nagy NB, Marei MK, Youssif MI. Transdifferentiation of bone marrow mesenchymal stem cells into neural cells via cerebrospinal fluid. Biomed Biotechnol. 2014;2(4):66-79.
Rad AA, Heidari MH, Aliaghaei A, Broujeni ME, Shojaei A, Abbaszadeh H-A. In vitro differentiation of adipose derived stem cells into functional dopaminergic neurons. Biomed Pharmacol J. 2017;10(2):595-605.