Induced Pluripotent Stem Cells and Genome-Editing Tools in Determining Gene Function and Therapy for Inherited Retinal Disorders
Abstract
:1. Introduction
2. Reprogramming Induced Pluripotent Stem Cells
Source of Patient Cells for iPSC Reprogramming
3. CRISPR/Cas9 Toolbox for iPSC Editing
3.1. CRISPR/Cas9 Editing System
3.2. Next-Generation Editing Tools: CRISPR Base and Prime Editors
3.3. Delivery of CRISPR/Cas9 Components to iPSC
4. CRISPR-Mediated iPSC Editing for Inherited Retinal Disorders
4.1. CRISPR Technology to Generate a “Human Disease Model in a Dish”
4.1.1. CRISPR-Mediated Gene Knockout in Human iPSC
4.1.2. CRISPR/Cas9 HDR to Generate Isogenic Corrected Human iPSC as Controls
4.1.3. CRISPR/Cas9-Mediated NHEJ to Target Mutated Allele in Patient-Derived iPSC
4.1.4. CRISPR Technology to Generate Mutated Human iPSC
4.2. CRISPR Technology to Model Retinal Development
4.3. Gene-Edited iPSC Differentiated into Retinal Cells for Transplantation
Publication | iPSC Source | Retinal Disease | Gene; Mutation; Patient Information | CRISPR-Mediated Genome Editing: Mechanism and Delivery |
---|---|---|---|---|
Bassuk et al., 2016 [98] | Dermal skin fibroblasts | XLRP | RPGR c.3070G>T | HDR correction of mutation. Transfection with plasmid for SpCas9 and gRNA expression and ssODN template. |
Burnight et al., 2017 [107] | Dermal skin fibroblasts | RP, LCA10 | 353-bp Alu insertion in MAK (Patient 1) CEP290 c.2991 + 1655 A>G, IVS26 (Patient 2–4) RHO c.163 C>A (Patient 5) | HDR correction of mutation 353-bp Alu insertion in MAK, by nucleofection with plasmids for SpCas9 and gRNA expression and HDR template. NHEJ-mediated repair and HDR correction of IVS26 mutation, by transfection of plasmids for SpCas9 or SaCas9 and single or dual gRNA expression. Knockout and HDR correction of RHO c.163 C>A. |
Buskin et al., 2018 [102] | Dermal skin fibroblasts | RP11 | PRPF31 c.1115_1125 del11 (Patient 1–3) PRPF31 c.522_527+10del (Patient 4) | HDR correction of c.1115_1125 del11 mutation in a patient-specific iPSC line. Transfection of plasmid for SpCas9 and gRNA expression and ssODN template. |
Deng et al., 2018 [99] | Renal epithelial cells | XLRP | RPGR c.1685_1686delAT (Patient 1) RPGR c.2234_2235delGA (Patient 2) RPGR c.2403_2404delAG (Patient 3) | HDR correction of c.1685_1686delAT mutation. Nucleofection with plasmids for SpCas9 and gRNA expression and HDR template. |
Foltz et al., 2018 [100] | Dermal skin fibroblasts | RP13 | PRPF8 c.6901C>T | HDR correction of mutation. Electroporation with plasmids for gRNA expression, Cas9-Gem mRNA and ssODN template. |
Gagliardi et al., 2018 [120] | Retinal Müller glial cells | / | AAVS1 | CRISPR-mediated HDR to introduce a reporter gene under the control of murine Crx promoter, in AAVS1 site. Transfection with plasmids for SpCas9 and gRNA expression and HDR template. |
Artero-Castro et al., 2019 [104] | Dermal skin fibroblasts | arRP | MERTK c.992_993delCA | HDR correction of mutation. Transfection with eSpCas9_1.1 RNP and ssODN template. Clones carrying homozygous and heterozygous correction were obtained. |
Bohrer et al., 2019 [108] | Dermal skin fibroblasts | ESCS | NR2E3 c.119-2A>C (Patient 1) NR2E3 c.219G>C and c.932G>A (Patient 2) | HDR correction of c.119-2A>C (Patient 1) and c.219G>C (Patient 2) mutations. Transfection with plasmids for SpCas9 and gRNA expression and HDR template. |
Brydon et al., 2019 [115] | Dermal skin fibroblasts | RP11 | PRPF31 exon 7 (Healthy donor) PRPF31 c.1115_1125del11(Patient) | Knockout of PRPF31 by targeting exon 7 in wt iPSC to create a haploinsufficient PRPF31+/- line, by nucleofection with plasmids for SpCas9 and gRNA expression. RP11-iPSC line carrying c.1115_1125 del11 mutation and corrected by CRISPR-mediated HDR (Buskin et al., 2018). |
Huang et al., 2019 [106] | PBMC | XLRS | RS1 c.625C>T (Patient 1) RS1 c.488G>A (Patient 2) | Correction of c.625C>T mutation in patient iPSC by CRISPR-mediated HDR and also an adenine base editing approach. Introduction of c.625C>T mutation in wt iPSC. Nucleofection of plasmids for Cas9, gRNA and HDR templates and ABE7.10 base editor. |
Kanzaki et al., 2020 [29] | Dental pulp cells | LCA16 | KCNJ13 | Knockout of KCNJ13 by targeting exon 2 and 3 in wt iPSC. Electroporation with SpCas9 protein and gRNA expression. |
Lam et al., 2020 [117] | Dermal skin fibroblasts | / | VSX2 BRN3b RCVRN | CRISPR-mediated HDR to introduce reporter genes in targeted loci. Transfection with plasmids for SpCas9 and gRNA expression and HDR templates. |
Lane et al., 2020 [116] | Dermal skin fibroblasts | XLRP | RP2 exon 2 RP2 c.358C>T | Knockout of RP2 by targeting exon 2 in wt iPSC. Electroporation with plasmid for SpCas9 and gRNA expression. |
Sanjurjo-Soriano et al., 2020 [109] | Dermal skin fibroblasts | USH2A | USH2A c.2299delG (Patient 1) USH2A c.2276G>T and c.2299delG (Patient 2) | HDR correction of USH2A mutations. Nucleofection with plasmid for eSpCas9(1.1) and ssODN template. |
Yang et al., 2020 [114] | PBMC | XLRS | RS1 | Introduction of RS1 c.625C>T in wt iPSC. Nanodiamond carriers of linear DNA for CRISPR components and HDR template. |
Artero-Castro et al., 2021 [105] | Dermal skin fibroblasts | arRP | MERTK c.992_993delCA | iPSC lines carrying c.992_993delCA mutation and homozygously or heterozygously corrected by CRISPR-mediated HDR (Artero-Castro et al., 2019). |
Chirco et al., 2021 [113] | PBMC | LCA7 | CRX c.464_465insGGCA CRX c.262A>C | Knockout of CRX c.262A>C mutated allele. Transfection with plasmids for SpCas9 and gRNA expression. |
Diakatou et al., 2021 [112] | Dermal skin fibroblasts | adRP | NR2E3 c.166G>A | Knockout of NR2E3 mutated allele. Transfection with plasmid for SpCas9 and mutation-specific gRNA expression. |
Liu et al., 2021 [110] | PBMC | USH2A | USH2A c.2299delG and c.1256G>T | HDR correction of USH2A c.2299delG mutation. Transfection with SpCas9 RNP and ssODN template. |
Matsuyama et al., 2021 [119] | Murine fibroblasts | / | Bhlhb4 Islet1 | Knockout of Bhlhb4 and Islet1 in Tg(Nrl-GFP); Ribeye-reporter miPS cells and Thy1-GCaMP6f; Ribeye-reporter mES cells. Nucleofection with plasmids for SpCas9 and gRNA expression. |
Wahlin et al, 2021 [118] | Fibroblasts | / | SIX6 POU4F2 | CRISPR-mediated HDR to introduce reporter genes in targeted loci. Transfection with plasmids for SpCas9 and gRNA expression and HDR templates. |
Cheng et al., 2022 [97] | Dermal skin fibroblasts | ODDD | CX43 | Knockout of CX43 in wt iPSC. Nucleofection with plasmid for SpCas9 protein and gRNA expression. |
Guan et al., 2022 [121] | Bone marrow CD34+ cells | / | RCVRN | CRISPR-mediated HDR to introduce a reporter gene in the targeted locus. Transfection with plasmids for SpCas9 and gRNA expression and HDR template. |
Georgiou et al., 2022 [103] | Dermal skin fibroblasts | RP11 | PRPF31 c.1115_1125 del11 (Patient 1–3) c.522_527+10del (Patient 4) | RP11-iPSC line carrying c.1115_1125 del11 mutation and corrected by CRISPR-mediated HDR (Buskin et al., 2018). |
Leung et al., 2022 [111] | Renal epithelial cells | LCA4 | AIPL1 c.834G>A (Patients 1) AIPL1 c.834G>A and c.466-1G>C (Patients 2–3) AIPL1 c.834G>A and c.665G>A (Patients 4) | HDR correction of mutation to create isogenic control lines. Nucleofection with eSpCas9_1.1 RNP and ssODN template. |
5. Concluding Remarks
Author Contributions
Funding
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Alcalde, I.; Sanchez-Fernandez, C.; Martin, C.; De Pablo, N.; Jemni-Damer, N.; Guinea, G.V.; Merayo-Lloves, J.; Del Olmo-Aguado, S. Human Stem Cell Transplantation for Retinal Degenerative Diseases: Where Are We Now? Medicina 2022, 58, 102. [Google Scholar] [CrossRef]
- Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131, 861–872. [Google Scholar] [CrossRef] [Green Version]
- Li, M.; Izpisua Belmonte, J.C. Looking to the future following 10 years of induced pluripotent stem cell technologies. Nat. Protoc. 2016, 11, 1579–1585. [Google Scholar] [CrossRef]
- Clevers, H. Modeling Development and Disease with Organoids. Cell 2016, 165, 1586–1597. [Google Scholar] [CrossRef] [Green Version]
- Duong, T.T.; Vasireddy, V.; Mills, J.A.; Bennett, J. Retinas in a Dish Peek into Inherited Retinal Degeneration. Cell Stem Cell 2016, 18, 688–689. [Google Scholar] [CrossRef] [Green Version]
- Ovando-Roche, P.; Georgiadis, A.; Smith, A.J.; Pearson, R.A.; Ali, R.R. Harnessing the Potential of Human Pluripotent Stem Cells and Gene Editing for the Treatment of Retinal Degeneration. Curr. Stem Cell Rep. 2017, 3, 112–123. [Google Scholar] [CrossRef] [Green Version]
- Poon, A.; Zhang, Y.; Chandrasekaran, A.; Phanthong, P.; Schmid, B.; Nielsen, T.T.; Freude, K.K. Modeling neurodegenerative diseases with patient-derived induced pluripotent cells: Possibilities and challenges. New Biotechnol. 2017, 39, 190–198. [Google Scholar] [CrossRef]
- Takahashi, K.; Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126, 663–676. [Google Scholar] [CrossRef] [Green Version]
- Hong, H.; Takahashi, K.; Ichisaka, T.; Aoi, T.; Kanagawa, O.; Nakagawa, M.; Okita, K.; Yamanaka, S. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009, 460, 1132–1135. [Google Scholar] [CrossRef] [Green Version]
- Liao, B.; Bao, X.; Liu, L.; Feng, S.; Zovoilis, A.; Liu, W.; Xue, Y.; Cai, J.; Guo, X.; Qin, B.; et al. MicroRNA cluster 302-367 enhances somatic cell reprogramming by accelerating a mesenchymal-to-epithelial transition. J. Biol. Chem. 2011, 286, 17359–17364. [Google Scholar] [CrossRef]
- Subramanyam, D.; Lamouille, S.; Judson, R.L.; Liu, J.Y.; Bucay, N.; Derynck, R.; Blelloch, R. Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat. Biotechnol. 2011, 29, 443–448. [Google Scholar] [CrossRef]
- Nakagawa, M.; Takizawa, N.; Narita, M.; Ichisaka, T.; Yamanaka, S. Promotion of direct reprogramming by transformation-deficient Myc. Proc. Natl. Acad. Sci. USA 2010, 107, 14152–14157. [Google Scholar] [CrossRef] [Green Version]
- Sommer, C.A.; Stadtfeld, M.; Murphy, G.J.; Hochedlinger, K.; Kotton, D.N.; Mostoslavsky, G. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 2009, 27, 543–549. [Google Scholar] [CrossRef] [Green Version]
- Stadtfeld, M.; Nagaya, M.; Utikal, J.; Weir, G.; Hochedlinger, K. Induced pluripotent stem cells generated without viral integration. Science 2008, 322, 945–949. [Google Scholar] [CrossRef] [Green Version]
- Fusaki, N.; Ban, H.; Nishiyama, A.; Saeki, K.; Hasegawa, M. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2009, 85, 348–362. [Google Scholar] [CrossRef] [Green Version]
- Okita, K.; Matsumura, Y.; Sato, Y.; Okada, A.; Morizane, A.; Okamoto, S.; Hong, H.; Nakagawa, M.; Tanabe, K.; Tezuka, K.; et al. A more efficient method to generate integration-free human iPS cells. Nat. Methods 2011, 8, 409–412. [Google Scholar] [CrossRef] [Green Version]
- Kogut, I.; McCarthy, S.M.; Pavlova, M.; Astling, D.P.; Chen, X.; Jakimenko, A.; Jones, K.L.; Getahun, A.; Cambier, J.C.; Pasmooij, A.M.G.; et al. High-efficiency RNA-based reprogramming of human primary fibroblasts. Nat. Commun. 2018, 9, 745. [Google Scholar] [CrossRef] [Green Version]
- Mandal, P.K.; Rossi, D.J. Reprogramming human fibroblasts to pluripotency using modified mRNA. Nat. Protoc. 2013, 8, 568–582. [Google Scholar] [CrossRef]
- Okita, K.; Yamakawa, T.; Matsumura, Y.; Sato, Y.; Amano, N.; Watanabe, A.; Goshima, N.; Yamanaka, S. An efficient nonviral method to generate integration-free human-induced pluripotent stem cells from cord blood and peripheral blood cells. Stem Cells 2013, 31, 458–466. [Google Scholar] [CrossRef]
- Staerk, J.; Dawlaty, M.M.; Gao, Q.; Maetzel, D.; Hanna, J.; Sommer, C.A.; Mostoslavsky, G.; Jaenisch, R. Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 2010, 7, 20–24. [Google Scholar] [CrossRef]
- Xue, Y.; Cai, X.; Wang, L.; Liao, B.; Zhang, H.; Shan, Y.; Chen, Q.; Zhou, T.; Li, X.; Hou, J.; et al. Generating a non-integrating human induced pluripotent stem cell bank from urine-derived cells. PLoS ONE 2013, 8, e70573. [Google Scholar] [CrossRef]
- Zhou, T.; Benda, C.; Dunzinger, S.; Huang, Y.; Ho, J.C.; Yang, J.; Wang, Y.; Zhang, Y.; Zhuang, Q.; Li, Y.; et al. Generation of human induced pluripotent stem cells from urine samples. Nat. Protoc. 2012, 7, 2080–2089. [Google Scholar] [CrossRef]
- Capowski, E.E.; Samimi, K.; Mayerl, S.J.; Phillips, M.J.; Pinilla, I.; Howden, S.E.; Saha, J.; Jansen, A.D.; Edwards, K.L.; Jager, L.D.; et al. Reproducibility and staging of 3D human retinal organoids across multiple pluripotent stem cell lines. Development 2019, 146, dev171686. [Google Scholar] [CrossRef] [Green Version]
- Foltz, L.P.; Clegg, D.O. Patient-derived induced pluripotent stem cells for modelling genetic retinal dystrophies. Prog. Retin. Eye Res. 2019, 68, 54–66. [Google Scholar] [CrossRef]
- Afanasyeva, T.A.V.; Corral-Serrano, J.C.; Garanto, A.; Roepman, R.; Cheetham, M.E.; Collin, R.W.J. A look into retinal organoids: Methods, analytical techniques, and applications. Cell. Mol. Life Sci. 2021, 78, 6505–6532. [Google Scholar] [CrossRef]
- Lane, A.; Philip, L.R.; Ruban, L.; Fynes, K.; Smart, M.; Carr, A.; Mason, C.; Coffey, P. Engineering efficient retinal pigment epithelium differentiation from human pluripotent stem cells. Stem Cells Transl. Med. 2014, 3, 1295–1304. [Google Scholar] [CrossRef]
- Geng, Z.; Walsh, P.J.; Truong, V.; Hill, C.; Ebeling, M.; Kapphahn, R.J.; Montezuma, S.R.; Yuan, C.; Roehrich, H.; Ferrington, D.A.; et al. Generation of retinal pigmented epithelium from iPSCs derived from the conjunctiva of donors with and without age related macular degeneration. PLoS ONE 2017, 12, e0173575. [Google Scholar] [CrossRef] [Green Version]
- Yoshida, T.; Ozawa, Y.; Suzuki, K.; Yuki, K.; Ohyama, M.; Akamatsu, W.; Matsuzaki, Y.; Shimmura, S.; Mitani, K.; Tsubota, K.; et al. The use of induced pluripotent stem cells to reveal pathogenic gene mutations and explore treatments for retinitis pigmentosa. Mol. Brain 2014, 7, 45. [Google Scholar] [CrossRef] [Green Version]
- Kanzaki, Y.; Fujita, H.; Sato, K.; Hosokawa, M.; Matsumae, H.; Shiraga, F.; Morizane, Y.; Ohuchi, H. KCNJ13 Gene Deletion Impairs Cell Alignment and Phagocytosis in Retinal Pigment Epithelium Derived from Human-Induced Pluripotent Stem Cells. Investig. Ophthalmol. Vis. Sci. 2020, 61, 38. [Google Scholar] [CrossRef]
- Slembrouck-Brec, A.; Rodrigues, A.; Rabesandratana, O.; Gagliardi, G.; Nanteau, C.; Fouquet, S.; Thuret, G.; Reichman, S.; Orieux, G.; Goureau, O. Reprogramming of Adult Retinal Muller Glial Cells into Human-Induced Pluripotent Stem Cells as an Efficient Source of Retinal Cells. Stem Cells Int. 2019, 2019, 7858796. [Google Scholar] [CrossRef]
- Gaj, T.; Gersbach, C.A.; Barbas, C.F., 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013, 31, 397–405. [Google Scholar] [CrossRef] [Green Version]
- Hockemeyer, D.; Soldner, F.; Beard, C.; Gao, Q.; Mitalipova, M.; DeKelver, R.C.; Katibah, G.E.; Amora, R.; Boydston, E.A.; Zeitler, B.; et al. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol. 2009, 27, 851–857. [Google Scholar] [CrossRef] [Green Version]
- Soldner, F.; Laganiere, J.; Cheng, A.W.; Hockemeyer, D.; Gao, Q.; Alagappan, R.; Khurana, V.; Golbe, L.I.; Myers, R.H.; Lindquist, S.; et al. Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 2011, 146, 318–331. [Google Scholar] [CrossRef] [Green Version]
- Yusa, K.; Rashid, S.T.; Strick-Marchand, H.; Varela, I.; Liu, P.Q.; Paschon, D.E.; Miranda, E.; Ordonez, A.; Hannan, N.R.; Rouhani, F.J.; et al. Targeted gene correction of alpha1-antitrypsin deficiency in induced pluripotent stem cells. Nature 2011, 478, 391–394. [Google Scholar] [CrossRef] [Green Version]
- Zou, J.; Maeder, M.L.; Mali, P.; Pruett-Miller, S.M.; Thibodeau-Beganny, S.; Chou, B.K.; Chen, G.; Ye, Z.; Park, I.H.; Daley, G.Q.; et al. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 2009, 5, 97–110. [Google Scholar] [CrossRef] [Green Version]
- Frank, S.; Skryabin, B.V.; Greber, B. A modified TALEN-based system for robust generation of knock-out human pluripotent stem cell lines and disease models. BMC Genom. 2013, 14, 773. [Google Scholar] [CrossRef] [Green Version]
- Hockemeyer, D.; Wang, H.; Kiani, S.; Lai, C.S.; Gao, Q.; Cassady, J.P.; Cost, G.J.; Zhang, L.; Santiago, Y.; Miller, J.C.; et al. Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 2011, 29, 731–734. [Google Scholar] [CrossRef] [Green Version]
- Ru, R.; Yao, Y.; Yu, S.; Yin, B.; Xu, W.; Zhao, S.; Qin, L.; Chen, X. Targeted genome engineering in human induced pluripotent stem cells by penetrating TALENs. Cell Regen. 2013, 2, 5. [Google Scholar] [CrossRef] [Green Version]
- Yang, L.; Guell, M.; Byrne, S.; Yang, J.L.; De Los Angeles, A.; Mali, P.; Aach, J.; Kim-Kiselak, C.; Briggs, A.W.; Rios, X.; et al. Optimization of scarless human stem cell genome editing. Nucleic Acids Res. 2013, 41, 9049–9061. [Google Scholar] [CrossRef]
- Mojica, F.J.; Diez-Villasenor, C.; Garcia-Martinez, J.; Soria, E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 2005, 60, 174–182. [Google Scholar] [CrossRef]
- Hsu, P.D.; Lander, E.S.; Zhang, F. Development and applications of CRISPR-Cas9 for genome engineering. Cell 2014, 157, 1262–1278. [Google Scholar] [CrossRef] [Green Version]
- Komor, A.C.; Zhao, K.T.; Packer, M.S.; Gaudelli, N.M.; Waterbury, A.L.; Koblan, L.W.; Kim, Y.B.; Badran, A.H.; Liu, D.R. Improved base excision repair inhibition and bacteriophage Mu Gam protein yields C:G-to-T:A base editors with higher efficiency and product purity. Sci. Adv. 2017, 3, eaao4774. [Google Scholar] [CrossRef] [Green Version]
- Makarova, K.S.; Wolf, Y.I.; Iranzo, J.; Shmakov, S.A.; Alkhnbashi, O.S.; Brouns, S.J.J.; Charpentier, E.; Cheng, D.; Haft, D.H.; Horvath, P.; et al. Evolutionary classification of CRISPR-Cas systems: A burst of class 2 and derived variants. Nat. Rev. Microbiol. 2020, 18, 67–83. [Google Scholar] [CrossRef]
- Jinek, M.; Chylinski, K.; Fonfara, I.; Hauer, M.; Doudna, J.A.; Charpentier, E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337, 816–821. [Google Scholar] [CrossRef]
- Bassett, A.R. Editing the genome of hiPSC with CRISPR/Cas9: Disease models. Mamm. Genome 2017, 28, 348–364. [Google Scholar] [CrossRef] [Green Version]
- Scully, R.; Panday, A.; Elango, R.; Willis, N.A. DNA double-strand break repair-pathway choice in somatic mammalian cells. Nat. Rev. Mol. Cell Biol. 2019, 20, 698–714. [Google Scholar] [CrossRef]
- Koike-Yusa, H.; Li, Y.; Tan, E.P.; Velasco-Herrera Mdel, C.; Yusa, K. Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat. Biotechnol. 2014, 32, 267–273. [Google Scholar] [CrossRef]
- van Overbeek, M.; Capurso, D.; Carter, M.M.; Thompson, M.S.; Frias, E.; Russ, C.; Reece-Hoyes, J.S.; Nye, C.; Gradia, S.; Vidal, B.; et al. DNA Repair Profiling Reveals Nonrandom Outcomes at Cas9-Mediated Breaks. Mol. Cell 2016, 63, 633–646. [Google Scholar] [CrossRef] [Green Version]
- Allen, F.; Crepaldi, L.; Alsinet, C.; Strong, A.J.; Kleshchevnikov, V.; De Angeli, P.; Palenikova, P.; Khodak, A.; Kiselev, V.; Kosicki, M.; et al. Predicting the mutations generated by repair of Cas9-induced double-strand breaks. Nat. Biotechnol. 2019, 37, 64–72. [Google Scholar] [CrossRef]
- Leenay, R.T.; Aghazadeh, A.; Hiatt, J.; Tse, D.; Roth, T.L.; Apathy, R.; Shifrut, E.; Hultquist, J.F.; Krogan, N.; Wu, Z.; et al. Large dataset enables prediction of repair after CRISPR-Cas9 editing in primary T cells. Nat. Biotechnol. 2019, 37, 1034–1037. [Google Scholar] [CrossRef]
- Shen, M.W.; Arbab, M.; Hsu, J.Y.; Worstell, D.; Culbertson, S.J.; Krabbe, O.; Cassa, C.A.; Liu, D.R.; Gifford, D.K.; Sherwood, R.I. Predictable and precise template-free CRISPR editing of pathogenic variants. Nature 2018, 563, 646–651. [Google Scholar] [CrossRef]
- Patrizi, C.; Llado, M.; Benati, D.; Iodice, C.; Marrocco, E.; Guarascio, R.; Surace, E.M.; Cheetham, M.E.; Auricchio, A.; Recchia, A. Allele-specific editing ameliorates dominant retinitis pigmentosa in a transgenic mouse model. Am. J. Hum. Genet. 2021, 108, 295–308. [Google Scholar] [CrossRef]
- Takata, M.; Sasaki, M.S.; Sonoda, E.; Morrison, C.; Hashimoto, M.; Utsumi, H.; Yamaguchi-Iwai, Y.; Shinohara, A.; Takeda, S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 1998, 17, 5497–5508. [Google Scholar] [CrossRef] [Green Version]
- Merkle, F.T.; Neuhausser, W.M.; Santos, D.; Valen, E.; Gagnon, J.A.; Maas, K.; Sandoe, J.; Schier, A.F.; Eggan, K. Efficient CRISPR-Cas9-mediated generation of knockin human pluripotent stem cells lacking undesired mutations at the targeted locus. Cell Rep. 2015, 11, 875–883. [Google Scholar] [CrossRef] [Green Version]
- Mali, P.; Yang, L.; Esvelt, K.M.; Aach, J.; Guell, M.; DiCarlo, J.E.; Norville, J.E.; Church, G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339, 823–826. [Google Scholar] [CrossRef] [Green Version]
- Paquet, D.; Kwart, D.; Chen, A.; Sproul, A.; Jacob, S.; Teo, S.; Olsen, K.M.; Gregg, A.; Noggle, S.; Tessier-Lavigne, M. Efficient introduction of specific homozygous and heterozygous mutations using CRISPR/Cas9. Nature 2016, 533, 125–129. [Google Scholar] [CrossRef]
- Hu, J.H.; Miller, S.M.; Geurts, M.H.; Tang, W.; Chen, L.; Sun, N.; Zeina, C.M.; Gao, X.; Rees, H.A.; Lin, Z.; et al. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature 2018, 556, 57–63. [Google Scholar] [CrossRef]
- Miller, S.M.; Wang, T.; Randolph, P.B.; Arbab, M.; Shen, M.W.; Huang, T.P.; Matuszek, Z.; Newby, G.A.; Rees, H.A.; Liu, D.R. Continuous evolution of SpCas9 variants compatible with non-G PAMs. Nat. Biotechnol. 2020, 38, 471–481. [Google Scholar] [CrossRef]
- Nishimasu, H.; Shi, X.; Ishiguro, S.; Gao, L.; Hirano, S.; Okazaki, S.; Noda, T.; Abudayyeh, O.O.; Gootenberg, J.S.; Mori, H.; et al. Engineered CRISPR-Cas9 nuclease with expanded targeting space. Science 2018, 361, 1259–1262. [Google Scholar] [CrossRef]
- Walton, R.T.; Christie, K.A.; Whittaker, M.N.; Kleinstiver, B.P. Unconstrained genome targeting with near-PAMless engineered CRISPR-Cas9 variants. Science 2020, 368, 290–296. [Google Scholar] [CrossRef]
- Brookhouser, N.; Raman, S.; Potts, C.; Brafman, D.A. May I Cut in? Gene Editing Approaches in Human Induced Pluripotent Stem Cells. Cells 2017, 6, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, Y.; Cao, J.; Xiong, M.; Petersen, A.J.; Dong, Y.; Tao, Y.; Huang, C.T.; Du, Z.; Zhang, S.C. Engineering Human Stem Cell Lines with Inducible Gene Knockout using CRISPR/Cas9. Cell Stem Cell 2015, 17, 233–244. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giacalone, J.C.; Sharma, T.P.; Burnight, E.R.; Fingert, J.F.; Mullins, R.F.; Stone, E.M.; Tucker, B.A. CRISPR-Cas9-Based Genome Editing of Human Induced Pluripotent Stem Cells. Curr. Protoc. Stem Cell Biol. 2018, 44, 5B 7 1–5B 7 22. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.; Yang, L.; Grishin, D.; Rios, X.; Ye, L.Y.; Hu, Y.; Li, K.; Zhang, D.; Church, G.M.; Pu, W.T. Efficient, footprint-free human iPSC genome editing by consolidation of Cas9/CRISPR and piggyBac technologies. Nat. Protoc. 2017, 12, 88–103. [Google Scholar] [CrossRef] [PubMed]
- Yusa, K. Seamless genome editing in human pluripotent stem cells using custom endonuclease-based gene targeting and the piggyBac transposon. Nat. Protoc. 2013, 8, 2061–2078. [Google Scholar] [CrossRef]
- Richardson, C.D.; Ray, G.J.; DeWitt, M.A.; Curie, G.L.; Corn, J.E. Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nat. Biotechnol. 2016, 34, 339–344. [Google Scholar] [CrossRef]
- Bischoff, N.; Wimberger, S.; Maresca, M.; Brakebusch, C. Improving Precise CRISPR Genome Editing by Small Molecules: Is there a Magic Potion? Cells 2020, 9, 1318. [Google Scholar] [CrossRef]
- Fu, Y.; Foden, J.A.; Khayter, C.; Maeder, M.L.; Reyon, D.; Joung, J.K.; Sander, J.D. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 2013, 31, 822–826. [Google Scholar] [CrossRef] [Green Version]
- Kim, H.; Kim, J.S. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 2014, 15, 321–334. [Google Scholar] [CrossRef]
- Doench, J.G.; Fusi, N.; Sullender, M.; Hegde, M.; Vaimberg, E.W.; Donovan, K.F.; Smith, I.; Tothova, Z.; Wilen, C.; Orchard, R.; et al. Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat. Biotechnol. 2016, 34, 184–191. [Google Scholar] [CrossRef]
- Veres, A.; Gosis, B.S.; Ding, Q.; Collins, R.; Ragavendran, A.; Brand, H.; Erdin, S.; Cowan, C.A.; Talkowski, M.E.; Musunuru, K. Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 2014, 15, 27–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rees, H.A.; Liu, D.R. Base editing: Precision chemistry on the genome and transcriptome of living cells. Nat. Rev. Genet. 2018, 19, 770–788. [Google Scholar] [CrossRef] [PubMed]
- Komor, A.C.; Kim, Y.B.; Packer, M.S.; Zuris, J.A.; Liu, D.R. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 2016, 533, 420–424. [Google Scholar] [CrossRef] [Green Version]
- Gaudelli, N.M.; Komor, A.C.; Rees, H.A.; Packer, M.S.; Badran, A.H.; Bryson, D.I.; Liu, D.R. Programmable base editing of A*T to G*C in genomic DNA without DNA cleavage. Nature 2017, 551, 464–471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Anzalone, A.V.; Koblan, L.W.; Liu, D.R. Genome editing with CRISPR-Cas nucleases, base editors, transposases and prime editors. Nat. Biotechnol. 2020, 38, 824–844. [Google Scholar] [CrossRef]
- Koblan, L.W.; Arbab, M.; Shen, M.W.; Hussmann, J.A.; Anzalone, A.V.; Doman, J.L.; Newby, G.A.; Yang, D.; Mok, B.; Replogle, J.M.; et al. Efficient C*G-to-G*C base editors developed using CRISPRi screens, target-library analysis, and machine learning. Nat. Biotechnol. 2021, 39, 1414–1425. [Google Scholar] [CrossRef]
- Anzalone, A.V.; Randolph, P.B.; Davis, J.R.; Sousa, A.A.; Koblan, L.W.; Levy, J.M.; Chen, P.J.; Wilson, C.; Newby, G.A.; Raguram, A.; et al. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 2019, 576, 149–157. [Google Scholar] [CrossRef]
- Bak, R.O.; Dever, D.P.; Porteus, M.H. CRISPR/Cas9 genome editing in human hematopoietic stem cells. Nat. Protoc. 2018, 13, 358–376. [Google Scholar] [CrossRef] [Green Version]
- Dever, D.P.; Bak, R.O.; Reinisch, A.; Camarena, J.; Washington, G.; Nicolas, C.E.; Pavel-Dinu, M.; Saxena, N.; Wilkens, A.B.; Mantri, S.; et al. CRISPR/Cas9 beta-globin gene targeting in human haematopoietic stem cells. Nature 2016, 539, 384–389. [Google Scholar] [CrossRef]
- Martin, R.M.; Ikeda, K.; Cromer, M.K.; Uchida, N.; Nishimura, T.; Romano, R.; Tong, A.J.; Lemgart, V.T.; Camarena, J.; Pavel-Dinu, M.; et al. Highly Efficient and Marker-free Genome Editing of Human Pluripotent Stem Cells by CRISPR-Cas9 RNP and AAV6 Donor-Mediated Homologous Recombination. Cell Stem Cell 2019, 24, 821–828.e825. [Google Scholar] [CrossRef]
- Brookhouser, N.; Tekel, S.J.; Standage-Beier, K.; Nguyen, T.; Schwarz, G.; Wang, X.; Brafman, D.A. BIG-TREE: Base-Edited Isogenic hPSC Line Generation Using a Transient Reporter for Editing Enrichment. Stem Cell Rep. 2020, 14, 184–191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nami, F.; Ramezankhani, R.; Vandenabeele, M.; Vervliet, T.; Vogels, K.; Urano, F.; Verfaillie, C. Fast and Efficient Generation of Isogenic Induced Pluripotent Stem Cell Lines Using Adenine Base Editing. CRISPR J 2021, 4, 502–518. [Google Scholar] [CrossRef] [PubMed]
- Osborn, M.J.; Newby, G.A.; McElroy, A.N.; Knipping, F.; Nielsen, S.C.; Riddle, M.J.; Xia, L.; Chen, W.; Eide, C.R.; Webber, B.R.; et al. Base Editor Correction of COL7A1 in Recessive Dystrophic Epidermolysis Bullosa Patient-Derived Fibroblasts and iPSCs. J. Investig. Dermatol. 2020, 140, 338–347.e335. [Google Scholar] [CrossRef] [PubMed]
- Qi, T.; Wu, F.; Xie, Y.; Gao, S.; Li, M.; Pu, J.; Li, D.; Lan, F.; Wang, Y. Base Editing Mediated Generation of Point Mutations Into Human Pluripotent Stem Cells for Modeling Disease. Front. Cell Dev. Biol. 2020, 8, 590581. [Google Scholar] [CrossRef]
- Surun, D.; Schneider, A.; Mircetic, J.; Neumann, K.; Lansing, F.; Paszkowski-Rogacz, M.; Hanchen, V.; Lee-Kirsch, M.A.; Buchholz, F. Efficient Generation and Correction of Mutations in Human iPS Cells Utilizing mRNAs of CRISPR Base Editors and Prime Editors. Genes 2020, 11, 511. [Google Scholar] [CrossRef]
- Bharucha, N.; Ataam, J.A.; Gavidia, A.A.; Karakikes, I. Generation of AAVS1 integrated doxycycline-inducible CRISPR-Prime Editor human induced pluripotent stem cell line. Stem Cell Res 2021, 57, 102610. [Google Scholar] [CrossRef]
- Chemello, F.; Chai, A.C.; Li, H.; Rodriguez-Caycedo, C.; Sanchez-Ortiz, E.; Atmanli, A.; Mireault, A.A.; Liu, N.; Bassel-Duby, R.; Olson, E.N. Precise correction of Duchenne muscular dystrophy exon deletion mutations by base and prime editing. Sci. Adv. 2021, 7, eabg4910. [Google Scholar] [CrossRef]
- Eggenschwiler, R.; Gschwendtberger, T.; Felski, C.; Jahn, C.; Langer, F.; Sterneckert, J.; Hermann, A.; Luhmann, J.; Steinemann, D.; Haase, A.; et al. A selectable all-in-one CRISPR prime editing piggyBac transposon allows for highly efficient gene editing in human cell lines. Sci. Rep. 2021, 11, 22154. [Google Scholar] [CrossRef]
- Germain, P.L.; Testa, G. Taming Human Genetic Variability: Transcriptomic Meta-Analysis Guides the Experimental Design and Interpretation of iPSC-Based Disease Modeling. Stem Cell Rep. 2017, 8, 1784–1796. [Google Scholar] [CrossRef] [Green Version]
- Bock, C.; Proschold, T.; Krienitz, L. Updating the Genus Dictyosphaerium and Description of Mucidosphaerium Gen. Nov. (Trebouxiophyceae) Based on Morphological and Molecular Data(1). J. Phycol. 2011, 47, 638–652. [Google Scholar] [CrossRef]
- Boulting, G.L.; Kiskinis, E.; Croft, G.F.; Amoroso, M.W.; Oakley, D.H.; Wainger, B.J.; Williams, D.J.; Kahler, D.J.; Yamaki, M.; Davidow, L.; et al. A functionally characterized test set of human induced pluripotent stem cells. Nat. Biotechnol. 2011, 29, 279–286. [Google Scholar] [CrossRef] [PubMed]
- Sandoe, J.; Eggan, K. Opportunities and challenges of pluripotent stem cell neurodegenerative disease models. Nat. Neurosci. 2013, 16, 780–789. [Google Scholar] [CrossRef] [PubMed]
- Sterneckert, J.L.; Reinhardt, P.; Scholer, H.R. Investigating human disease using stem cell models. Nat. Rev. Genet. 2014, 15, 625–639. [Google Scholar] [CrossRef] [PubMed]
- Weiss, K.M.; Clark, A.G. Linkage disequilibrium and the mapping of complex human traits. Trends Genet. 2002, 18, 19–24. [Google Scholar] [CrossRef]
- Fuster-Garcia, C.; Garcia-Bohorquez, B.; Rodriguez-Munoz, A.; Millan, J.M.; Garcia-Garcia, G. Application of CRISPR Tools for Variant Interpretation and Disease Modeling in Inherited Retinal Dystrophies. Genes 2020, 11, 473. [Google Scholar] [CrossRef]
- McTague, A.; Rossignoli, G.; Ferrini, A.; Barral, S.; Kurian, M.A. Genome Editing in iPSC-Based Neural Systems: From Disease Models to Future Therapeutic Strategies. Front. Genome Ed. 2021, 3, 630600. [Google Scholar] [CrossRef]
- Cheng, L.; Cring, M.R.; Wadkins, D.A.; Kuehn, M.H. Absence of Connexin 43 Results in Smaller Retinas and Arrested, Depolarized Retinal Progenitor Cells in Human Retinal Organoids. Stem Cells 2022, 40, 592–604. [Google Scholar] [CrossRef]
- Bassuk, A.G.; Zheng, A.; Li, Y.; Tsang, S.H.; Mahajan, V.B. Precision Medicine: Genetic Repair of Retinitis Pigmentosa in Patient-Derived Stem Cells. Sci. Rep. 2016, 6, 19969. [Google Scholar] [CrossRef] [Green Version]
- Deng, W.L.; Gao, M.L.; Lei, X.L.; Lv, J.N.; Zhao, H.; He, K.W.; Xia, X.X.; Li, L.Y.; Chen, Y.C.; Li, Y.P.; et al. Gene Correction Reverses Ciliopathy and Photoreceptor Loss in iPSC-Derived Retinal Organoids from Retinitis Pigmentosa Patients. Stem Cell Rep. 2018, 10, 2005. [Google Scholar] [CrossRef]
- Foltz, L.P.; Howden, S.E.; Thomson, J.A.; Clegg, D.O. Functional Assessment of Patient-Derived Retinal Pigment Epithelial Cells Edited by CRISPR/Cas9. Int. J. Mol. Sci. 2018, 19, 4127. [Google Scholar] [CrossRef]
- Howden, S.E.; McColl, B.; Glaser, A.; Vadolas, J.; Petrou, S.; Little, M.H.; Elefanty, A.G.; Stanley, E.G. A Cas9 Variant for Efficient Generation of Indel-Free Knockin or Gene-Corrected Human Pluripotent Stem Cells. Stem Cell Rep. 2016, 7, 508–517. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buskin, A.; Zhu, L.; Chichagova, V.; Basu, B.; Mozaffari-Jovin, S.; Dolan, D.; Droop, A.; Collin, J.; Bronstein, R.; Mehrotra, S.; et al. Disrupted alternative splicing for genes implicated in splicing and ciliogenesis causes PRPF31 retinitis pigmentosa. Nat. Commun. 2018, 9, 4234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Georgiou, M.; Yang, C.; Atkinson, R.; Pan, K.T.; Buskin, A.; Molina, M.M.; Collin, J.; Al-Aama, J.; Goertler, F.; Ludwig, S.E.J.; et al. Activation of autophagy reverses progressive and deleterious protein aggregation in PRPF31 patient-induced pluripotent stem cell-derived retinal pigment epithelium cells. Clin. Transl. Med. 2022, 12, e759. [Google Scholar] [CrossRef]
- Artero Castro, A.; Long, K.; Bassett, A.; Machuca, C.; Leon, M.; Avila-Fernandez, A.; Corton, M.; Vidal-Puig, T.; Ayuso, C.; Lukovic, D.; et al. Generation of gene-corrected human induced pluripotent stem cell lines derived from retinitis pigmentosa patient with Ser331Cysfs*5 mutation in MERTK. Stem Cell Res 2019, 34, 101341. [Google Scholar] [CrossRef]
- Artero-Castro, A.; Long, K.; Bassett, A.; Avila-Fernandez, A.; Corton, M.; Vidal-Puig, A.; Jendelova, P.; Rodriguez-Jimenez, F.J.; Clemente, E.; Ayuso, C.; et al. Gene Correction Recovers Phagocytosis in Retinal Pigment Epithelium Derived from Retinitis Pigmentosa-Human-Induced Pluripotent Stem Cells. Int. J. Mol. Sci. 2021, 22, 2092. [Google Scholar] [CrossRef]
- Huang, K.C.; Wang, M.L.; Chen, S.J.; Kuo, J.C.; Wang, W.J.; Nhi Nguyen, P.N.; Wahlin, K.J.; Lu, J.F.; Tran, A.A.; Shi, M.; et al. Morphological and Molecular Defects in Human Three-Dimensional Retinal Organoid Model of X-Linked Juvenile Retinoschisis. Stem Cell Rep. 2019, 13, 906–923. [Google Scholar] [CrossRef]
- Burnight, E.R.; Gupta, M.; Wiley, L.A.; Anfinson, K.R.; Tran, A.; Triboulet, R.; Hoffmann, J.M.; Klaahsen, D.L.; Andorf, J.L.; Jiao, C.; et al. Using CRISPR-Cas9 to Generate Gene-Corrected Autologous iPSCs for the Treatment of Inherited Retinal Degeneration. Mol. Ther. J. Am. Soc. Gene Ther. 2017, 25, 1999–2013. [Google Scholar] [CrossRef] [Green Version]
- Bohrer, L.R.; Wiley, L.A.; Burnight, E.R.; Cooke, J.A.; Giacalone, J.C.; Anfinson, K.R.; Andorf, J.L.; Mullins, R.F.; Stone, E.M.; Tucker, B.A. Correction of NR2E3 Associated Enhanced S-cone Syndrome Patient-specific iPSCs using CRISPR-Cas9. Genes 2019, 10, 278. [Google Scholar] [CrossRef] [Green Version]
- Sanjurjo-Soriano, C.; Erkilic, N.; Baux, D.; Mamaeva, D.; Hamel, C.P.; Meunier, I.; Roux, A.F.; Kalatzis, V. Genome Editing in Patient iPSCs Corrects the Most Prevalent USH2A Mutations and Reveals Intriguing Mutant mRNA Expression Profiles. Mol. Methods Clin. Dev. 2020, 17, 156–173. [Google Scholar] [CrossRef] [Green Version]
- Liu, X.; Lillywhite, J.; Zhu, W.; Huang, Z.; Clark, A.M.; Gosstola, N.; Maguire, C.T.; Dykxhoorn, D.; Chen, Z.Y.; Yang, J. Generation and Genetic Correction of USH2A c.2299delG Mutation in Patient-Derived Induced Pluripotent Stem Cells. Genes 2021, 12, 805. [Google Scholar] [CrossRef]
- Leung, A.; Sacristan-Reviriego, A.; Perdigao, P.R.L.; Sai, H.; Georgiou, M.; Kalitzeos, A.; Carr, A.F.; Coffey, P.J.; Michaelides, M.; Bainbridge, J.; et al. Investigation of PTC124-mediated translational readthrough in a retinal organoid model of AIPL1-associated Leber congenital amaurosis. Stem Cell Rep. 2022, 17, 2187–2202. [Google Scholar] [CrossRef] [PubMed]
- Diakatou, M.; Dubois, G.; Erkilic, N.; Sanjurjo-Soriano, C.; Meunier, I.; Kalatzis, V. Allele-Specific Knockout by CRISPR/Cas to Treat Autosomal Dominant Retinitis Pigmentosa Caused by the G56R Mutation in NR2E3. Int. J. Mol. Sci. 2021, 22, 2607. [Google Scholar] [CrossRef] [PubMed]
- Chirco, K.R.; Chew, S.; Moore, A.T.; Duncan, J.L.; Lamba, D.A. Allele-specific gene editing to rescue dominant CRX-associated LCA7 phenotypes in a retinal organoid model. Stem Cell Rep. 2021, 16, 2690–2702. [Google Scholar] [CrossRef] [PubMed]
- Yang, T.C.; Chang, C.Y.; Yarmishyn, A.A.; Mao, Y.S.; Yang, Y.P.; Wang, M.L.; Hsu, C.C.; Yang, H.Y.; Hwang, D.K.; Chen, S.J.; et al. Carboxylated nanodiamond-mediated CRISPR-Cas9 delivery of human retinoschisis mutation into human iPSCs and mouse retina. Acta Biomater. 2020, 101, 484–494. [Google Scholar] [CrossRef]
- Brydon, E.M.; Bronstein, R.; Buskin, A.; Lako, M.; Pierce, E.A.; Fernandez-Godino, R. AAV-Mediated Gene Augmentation Therapy Restores Critical Functions in Mutant PRPF31(+/-) iPSC-Derived RPE Cells. Mol. Methods Clin. Dev. 2019, 15, 392–402. [Google Scholar] [CrossRef]
- Lane, A.; Jovanovic, K.; Shortall, C.; Ottaviani, D.; Panes, A.B.; Schwarz, N.; Guarascio, R.; Hayes, M.J.; Palfi, A.; Chadderton, N.; et al. Modeling and Rescue of RP2 Retinitis Pigmentosa Using iPSC-Derived Retinal Organoids. Stem Cell Rep. 2020, 15, 67–79. [Google Scholar] [CrossRef]
- Lam, P.T.; Gutierrez, C.; Del Rio-Tsonis, K.; Robinson, M.L. Generation of a Retina Reporter hiPSC Line to Label Progenitor, Ganglion, and Photoreceptor Cell Types. Transl. Vis. Sci. Technol. 2020, 9, 21. [Google Scholar] [CrossRef] [Green Version]
- Wahlin, K.J.; Cheng, J.; Jurlina, S.L.; Jones, M.K.; Dash, N.R.; Ogata, A.; Kibria, N.; Ray, S.; Eldred, K.C.; Kim, C.; et al. CRISPR Generated SIX6 and POU4F2 Reporters Allow Identification of Brain and Optic Transcriptional Differences in Human PSC-Derived Organoids. Front. Cell Dev. Biol. 2021, 9, 764725. [Google Scholar] [CrossRef]
- Matsuyama, T.; Tu, H.Y.; Sun, J.; Hashiguchi, T.; Akiba, R.; Sho, J.; Fujii, M.; Onishi, A.; Takahashi, M.; Mandai, M. Genetically engineered stem cell-derived retinal grafts for improved retinal reconstruction after transplantation. iScience 2021, 24, 102866. [Google Scholar] [CrossRef]
- Gagliardi, G.; Ben M’Barek, K.; Chaffiol, A.; Slembrouck-Brec, A.; Conart, J.B.; Nanteau, C.; Rabesandratana, O.; Sahel, J.A.; Duebel, J.; Orieux, G.; et al. Characterization and Transplantation of CD73-Positive Photoreceptors Isolated from Human iPSC-Derived Retinal Organoids. Stem Cell Rep. 2018, 11, 665–680. [Google Scholar] [CrossRef]
- Guan, Y.; Wang, Y.; Zheng, D.; Xie, B.; Xu, P.; Gao, G.; Zhong, X. Generation of an RCVRN-eGFP Reporter hiPSC Line by CRISPR/Cas9 to Monitor Photoreceptor Cell Development and Facilitate the Cell Enrichment for Transplantation. Front. Cell Dev. Biol. 2022, 10, 870441. [Google Scholar] [CrossRef] [PubMed]
Publication | iPSC Source | Reprogramming Method | Donor Info; Gene; Mutation |
---|---|---|---|
Yoshida et al., 2014 [28] | Dermal skin fibroblasts | Retroviral transduction | RP patient, RHO c.541G>A |
Geng et al., 2017 [27] | Conjunctival cells | Sendai virus | AMD patients and healthy donor |
Capowski et al., 2019 [23] | Blood/Fibroblasts | Episomal vectors | RP/LCA/Usher syndrome patients and healthy donors |
Slembrouck-Brec et al., 2019 [30] | Post-mortem adult Müller glia | Sendai virus | Healthy donor |
Kanzaki et al., 2020 [29] | Dental pulp cells | Episomal vectors | Healthy donor |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Benati, D.; Leung, A.; Perdigao, P.; Toulis, V.; van der Spuy, J.; Recchia, A. Induced Pluripotent Stem Cells and Genome-Editing Tools in Determining Gene Function and Therapy for Inherited Retinal Disorders. Int. J. Mol. Sci. 2022, 23, 15276. https://doi.org/10.3390/ijms232315276
Benati D, Leung A, Perdigao P, Toulis V, van der Spuy J, Recchia A. Induced Pluripotent Stem Cells and Genome-Editing Tools in Determining Gene Function and Therapy for Inherited Retinal Disorders. International Journal of Molecular Sciences. 2022; 23(23):15276. https://doi.org/10.3390/ijms232315276
Chicago/Turabian StyleBenati, Daniela, Amy Leung, Pedro Perdigao, Vasileios Toulis, Jacqueline van der Spuy, and Alessandra Recchia. 2022. "Induced Pluripotent Stem Cells and Genome-Editing Tools in Determining Gene Function and Therapy for Inherited Retinal Disorders" International Journal of Molecular Sciences 23, no. 23: 15276. https://doi.org/10.3390/ijms232315276