Genome engineering of stem cell organoids for disease modeling
Received date: 30 Nov 2016
Accepted date: 28 Dec 2016
Published date: 12 Jun 2017
Copyright
Precision medicine emerges as a new approach that takes into account individual variability. Successful realization of precision medicine requires disease models that are able to incorporate personalized disease information and recapitulate disease development processes at the molecular, cellular and organ levels. With recent development in stem cell field, a variety of tissue organoids can be derived from patient specific pluripotent stem cells and adult stem cells. In combination with the state-of-the-art genome editing tools, organoids can be further engineered to mimic diseaserelevant genetic and epigenetic status of a patient. This has therefore enabled a rapid expansion of sophisticated in vitro disease models, offering a unique system for fundamental and biomedical research as well as the development of personalized medicine. Here we summarize some of the latest advances and future perspectives in engineering stem cell organoids for human disease modeling.
Yingmin Sun , Qiurong Ding . Genome engineering of stem cell organoids for disease modeling[J]. Protein & Cell, 2017 , 8(5) : 315 -327 . DOI: 10.1007/s13238-016-0368-0
1 |
AiharaE, MaheMM, SchumacherMA, MatthisAL, FengR, RenW, NoahTK, Matsu-uraT, MooreSR, HongCI
|
2 |
AmabileA, MigliaraA, CapassoP, BiffiM, CittaroD, NaldiniL, LombardoA (2016) Inheritable silencing of endogenous genes by hit-and-run targeted epigenetic editing. Cell167:219–232
|
3 |
BarkerN, HuchM, KujalaP, van de WeteringM, SnippertHJ, van EsJH, SatoT, StangeDE, BegthelH, van den BornM
|
4 |
BartfeldS, BayramT, van de WeteringM, HuchM, BegthelH, KujalaP, VriesR, PetersPJ, CleversH (2015) In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection. Gastroenterology148:126–136
|
5 |
Ben-ZviD, MeltonDA (2015) Modeling human nutrition using human embryonic stem cells. Cell161:12–17
|
6 |
BigorgneAE, FarinHF, LemoineR, MahlaouiN, LambertN, GilM, SchulzA, PhilippetP, SchlesserP, AbrahamsenTG
|
7 |
BojSF, HwangCI, BakerLA, ChioII, EngleDD, CorboV, JagerM, Ponz-SarviseM, TiriacH, SpectorMS
|
8 |
CanverMC, SmithEC, SherF, PinelloL, SanjanaNE, ShalemO, ChenDD, SchuppPG, VinjamurDS, GarciaSP
|
9 |
ChenB, GilbertLA, CiminiBA, SchnitzbauerJ, ZhangW, LiGW, ParkJ, BlackburnEH, WeissmanJS, QiLS
|
10 |
ChenS, SanjanaNE, ZhengK, ShalemO, LeeK, ShiX, ScottDA, SongJ, PanJQ, WeisslederR
|
11 |
ChengAW, WangH, YangH, ShiL, KatzY, TheunissenTW, RangarajanS, ShivalilaCS, DadonDB, JaenischR (2013) Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res23:1163–1171
|
12 |
ChuaCW, ShibataM, LeiM, ToivanenR, BarlowLJ, BergrenSK, BadaniKK, McKiernanJM, BensonMC, HibshooshH
|
13 |
CollinsFS, VarmusH (2015) A new initiative on precision medicine. N Engl J Med372:793–795
|
14 |
DekkersJF, WiegerinckCL, de JongeHR, BronsveldI, JanssensHM, de Winter-de GrootKM, BrandsmaAM, de JongNW, BijveldsMJ, ScholteBJ
|
15 |
DeWardAD, CramerJ, LagasseE (2014) Celluar heterogeneity in the mouse esophagus implicates the presence of a nonquiescent epithelial stem cell population. Cell Rep9:701–711
|
16 |
DingQ, LeeYK, SchaeferEA, PetersDT, VeresA, KimK, KuperwasserN, MotolaDL, MeissnerTB, HendriksWT
|
17 |
DrostJ, van JaarsveldRH, PonsioenB, ZimberlinC, van BoxtelR, BuijsA, SachsN, OvermeerRM, OfferhausGJ, BegthelH
|
18 |
DyeBR, HillDR, FergusonMA, TsaiYH, NagyMS, DyalR, WellsJM, MayhewCN, NattivR, KleinOD
|
19 |
EirakuM, WatanabeK, Matsuo-TakasakiM, KawadaM, YonemuraS, MatsumuraM, WatayaT, NishiyamaA, MugurumaK, SasaiY (2008) Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell3:519–532
|
20 |
EirakuM, TakataN, IshibashiH, KawadaM, SakakuraE, OkudaS, SekiguchiK, AdachiT, SasaiY (2011) Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature472:51–56
|
21 |
ForbesterJL, GouldingD, VallierL, HannanN, HaleC, PickardD, MukhopadhyayS, DouganG (2015) Interaction of Salmonella enterica Serovar Typhimurium with intestinal organoids derived from human induced pluripotent stem cells. Infect Immun83:2926–2934
|
22 |
GaoD, VelaI, SbonerA, IaquintaPJ, KarthausWR, GopalanA, DowlingC, WanjalaJN, UndvallEA, AroraVK
|
23 |
GaspardN, BouschetT, HourezR, DimidschsteinJ, NaeijeG, van den AmeeleJ, Espuny-CamachoI, HerpoelA, PassanteL, SchiffmannSN
|
24 |
GilbertLA, LarsonMH, MorsutL, LiuZ, BrarGA, TorresSE, Stern-GinossarN, BrandmanO, WhiteheadEH, DoudnaJA
|
25 |
GilbertLA, HorlbeckMA, AdamsonB, VillaltaJE, ChenY, WhiteheadEH, GuimaraesC, PanningB, PloeghHL, BassikMC
|
26 |
HiltonIB, D’IppolitoAM, VockleyCM, ThakorePI, CrawfordGE, ReddyTE, GersbachCA (2015) Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol33:510–517
|
27 |
HishaH, TanakaT, KannoS, TokuyamaY, KomaiY, OheS, YanaiH, OmachiT, UenoH (2013) Establishment of a novel lingual organoid culture system: generation of organoids having mature keratinized epithelium from adult epithelial stem cells. Sci Rep3:3224
|
28 |
HsuPD, LanderES, ZhangF (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell157:1262–1278
|
29 |
HuchM, BonfantiP, BojSF, SatoT, LoomansCJ, van de WeteringM, SojoodiM, LiVS, SchuijersJ, GracaninA
|
30 |
HuchM, DorrellC, BojSF, van EsJH, LiVS, van de WeteringM, SatoT, HamerK, SasakiN, FinegoldMJ
|
31 |
HuchM, GehartH, van BoxtelR, HamerK, BlokzijlF, VerstegenMM, EllisE, van WenumM, FuchsSA, de LigtJ
|
32 |
JainIH, ZazzeronL, GoliR, AlexaK, Schatzman-BoneS, DhillonH, GoldbergerO, PengJ, ShalemO, SanjanaNE
|
33 |
JungP, SatoT, Merlos-SuárezA, BarrigaFM, IglesiasM, RossellD, AuerH, GallardoM, BlascoMA, SanchoE
|
34 |
KarthausWR, IaquintaPJ, DrostJ, GracaninA, van BoxtelR, WongvipatJ, DowlingCM, GaoD, BegthelH, SachsN
|
35 |
KearnsNA, PhamH, TabakB, GengaRM, SilversteinNJ, GarberM, MaehrR (2015) Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat Methods12:401–403
|
36 |
KoehlerKR, HashinoE (2014) 3D mouse embryonic stem cell culture for generating inner ear organoids. Nat Protoc9:1229–1244
|
37 |
KoehlerKR, MikoszAM, MoloshAI, PatelD, HashinoE (2013) Generation of inner ear sensory epithelia from pluripotent stem cells in 3D culture. Nature500:217–221
|
38 |
Koike-YusaH, LiY, TanEP, Velasco-Herrera MdelC, YusaK (2014) Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat Biotechnol32:267–273
|
39 |
KomorAC, KimYB, PackerMS, ZurisJA, LiuDR (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature533:420–424
|
40 |
KonermannS, BrighamMD, TrevinoAE, JoungJ, AbudayyehOO, BarcenaC, HsuPD, HabibN, GootenbergJS, NishimasuH
|
41 |
KubbenN, ZhangW, WangL, VossTC, YangJ, QuJ, LiuGH, MisteliT (2016) Repression of the antioxidant NRF2 pathway in premature aging. Cell165:1361–1374
|
42 |
LancasterMA, KnoblichJA (2014) Generation of cerebral organoids from human pluripotent stem cells. Nat Protoc9:2329–2340
|
43 |
LancasterMA, RennerM, MartinCA, WenzelD, BicknellLS, HurlesME, HomfrayT, PenningerJM, JacksonAP, KnoblichJA (2013) Cerebral organoids model human brain development and microcephaly. Nature501:373–379
|
44 |
LeeJH, BhangDH, BeedeA, HuangTL, StrippBR, BlochKD, WagersAJ, TsengYH, RyeomS, KimCF (2014) Lung stem cell differentiation in mice directed by endothelial cells via a BMP4-NFATc1-thrombospondin-1 axis. Cell156:440–455
|
45 |
LeslieJL, HuangS, OppJS, NagyMS, KobayashiM, YoungVB, SpenceJR (2015) Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect Immun83:138–145
|
46 |
LiY, ZhangW, ChangL, HanY, SunL, GongX, TangH, LiuZ, DengH, YeY (2016) Vitamin C alleviates aging defects in a stem cell model for Werner syndrome. Protein Cell7:478–488
|
47 |
LiuGH, SuzukiK, QuJ, Sancho-MartinezI, YiF, LiM, KumarS, NivetE, KimJ, SoligallaRD
|
48 |
MaH, TuLC, NaseriA, HuismanM, ZhangS, GrunwaldD, PedersonT (2016a) Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow. Nat Biotechnol34:528–530
|
49 |
MaY, ZhangJ, YinW, ZhangZ, SongY, ChangX (2016b) Targeted AID-mediated mutagenesis(TAM) enables efficient genomic diversification in mammalian cells. Nat Methods. doi:10.1038/nmeth.4027
|
50 |
MarianiJ, SimoniniMV, PalejevD, TomasiniL, CoppolaG, SzekelyAM, HorvathTL, VaccarinoFM (2012) Modeling human cortical development in vitro using induced pluripotent stem cells. Proc Nati Acad Sci USA109:12770–12775
|
51 |
MarianiJ, CoppolaG, ZhangP, AbyzovA, ProviniL, TomasiniL, AmenduniM, SzekelyA, PalejevD, WilsonM
|
52 |
MaschmeyerI, LorenzAK, SchimekK, HasenbergT, RammeAP, HübnerJ, LindnerM, DrewellC, BauerS, ThomasA
|
53 |
MatanoM, DateS, ShimokawaM, TakanoA, FujiiM, OhtaY, WatanabeT, KanaiT, SatoT (2015) Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids. Nat Med21:256–262
|
54 |
McCrackenKW, HowellJC, WellsJM, SpenceJR (2011) Generating human intestinal tissue from pluripotent stem cells in vitro. Nat Protoc6:1920–1928
|
55 |
McCrackenKW, CatáEM, CrawfordCM, SinagogaKL, SchumacherM, RockichBE, TsaiYH, MayhewCN, SpenceJR, ZavrosY
|
56 |
MondrinosMJ, KoutzakiS, JiwanmallE, LiM, DechadarevianJP, LelkesPI, FinckCM (2006) Engineering three-dimensional pulmonary tissue constructs. Tissue Eng12:717–728
|
57 |
MondrinosMJ, JonesPL, FinckCM, LelkesPI (2014) Engineering de novo assembly of fetal pulmonary organoids. Tissue Eng Part A20:2892–2907
|
58 |
MugurumaK, NishiyamaA, OnoY, MiyawakiH, MizuharaE, HoriS, KakizukaA, ObataK, YanagawaY, HiranoT
|
59 |
MugurumaK, NishiyamaA, KawakamiH, HashimotoK, SasaiY (2015) Self-organization of polarized cerebellar tissue in 3D culture of human pluripotent stem cells. Cell Rep10:537–550
|
60 |
MusunuruK (2013) Genome editing of human pluripotent stem cells to generate human cellular disease models. Dis Model Mech6:896–904
|
61 |
NanduriLS, BaanstraM, FaberH, RocchiC, ZwartE, de HaanG, van OsR, CoppesRP (2014) Purification and ex vivo expansion of fully functional salivary gland stem cells. Stem Cell Reports3:957–964
|
62 |
NellesDA, FangMY, O’ConnellMR, XuJL, MarkmillerSJ, DoudnaJA, YeoGW (2016) Programmable RNA tracking in live cells with CRISPR/Cas9. Cell165:488–496
|
63 |
NishidaK, ArazoeT, YachieN, BannoS, KakimotoM, TabataM, MochizukiM, MiyabeA, ArakiM, HaraKY
|
64 |
NoguchiTK, NinomiyaN, SekineM, KomazakiS, WangPC, AsashimaM, KurisakiA (2015) Generation of stomch tissue from mosue embryonic stem cell. Nat Cell Biol17:984–993
|
65 |
OgawaM, OgawaS, BearCE, AhmadiS, ChinS, LiB, GrompeM, KellerG, KamathBM, GhanekarA (2015) Directed differentiation of cholangiocytes from human pluripotent stem cells. Nat Biotechnol33:853–861
|
66 |
OotaniA, LiX, SangiorgiE, HoQT, UenoH, TodaS, SugiharaH, FujimotoK, WeissmanIL, CapecchiMR
|
67 |
OzoneC, SugaH, EirakuM, KadoshimaT, YonemuraS, TakataN, OisoY, TsujiT, SasaiY (2016) Functional anterior pituitary generated in self-organizing culture of human embryonic stem cells. Nat Commun7:10351
|
68 |
ParnasO, JovanovicM, EisenhaureTM, HerbstRH, DixitA, YeCJ, PrzybylskiD, PlattRJ, TiroshI, SanjanaNE
|
69 |
Perez-PineraP, KocakDD, VockleyCM, AdlerAF, KabadiAM, PolsteinLR, ThakorePI, GlassKA, OusteroutDG, LeongKW
|
70 |
Perez-PineraP, OusteroutDG, BrungerJM, FarinAM, GlassKA, GuilakF, CrawfordGE, HarteminkAJ, GersbachCA (2013b) Synergistic and tunable human gene activation by combinations of synthetic transcription factors. Nat Methods10:239–242
|
71 |
QiLS, LarsonMH, GilbertLA, DoudnaJA, WeissmanJS, ArkinAP, LimWA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell152:1173–1183
|
72 |
QianX, NguyenHN, SongMM, HadionoC, OgdenSC, HammackC, YaoB, HamerskyGR, JacobF, ZhongC
|
73 |
RenW, LewandowskiBC, WatsonJ, AiharaE, IwatsukiK, BachmanovAA, MargolskeeRF, JiangP (2014) Single Lgr5- or Lgr6- expressing taste stem/progenitor cells generate taste bud cells ex vivo. Proc Natl Acad Sci USA111:16401–16406
|
74 |
SampaziotisF, Cardoso de BritoM, MadrigalP, BerteroA, Saeb-ParsyK, SoaresFA, SchrumpfE, MelumE, KarlsenTH, BradleyJA
|
75 |
SanjanaNE, WrightJ, ZhengK, ShalemO, FontanillasP, JoungJ, ChengC, RegevA, ZhangF (2016) High-resolution interrogation of functional elements in the noncoding genome. Science353:1545–1549
|
76 |
SatoT, VriesRG, SnippertHJ, van de WeteringM, BarkerN, StangeDE, van EsJH, AboA, KujalaP, PetersPJ
|
77 |
SatoT, StangeDE, FerranteM, VriesRG, Van EsJH, Van den BrinkS, Van HoudtWJ, PronkA, Van GorpJ
|
78 |
SchlaermannP, ToelleB, BergerH, SchmidtSC, GlanemannM, OrdemannJ, BartfeldS, MollenkopfHJ, MeyerTF (2016) A novel human gastric primary cell culture system for modeling Helicobacter pylori infection in vitro. Gut65:201–213
|
79 |
SchmidtJC, ZaugAJ, CechTR (2016) Live cell imaging reveals the dynamics of telomerase recruitment to telomeres. Cell166:1188–1197
|
80 |
SchweigerPJ, JensenKB (2016) Modeling human disease using organotypic cultures. Curr Opin Cell Biol43:22–29
|
81 |
ShalemO, SanjanaNE, HartenianE, ShiX, ScottDA, MikkelsenTS, HecklD, EbertBL, RootDE, DoenchJG
|
82 |
ShiJ, ZhaoY, WangK, ShiX, WangY, HuangH, ZhuangY, CaiT, WangF, ShaoF (2015) Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature526:660–665
|
83 |
SpenceJR, MayhewCN, RankinSA, KuharMF, VallanceJE, TolleK, HoskinsEE, KalinichenkoVV, WellsSI, ZornAM
|
84 |
StangeDE, KooBK, HuchM, SibbelG, BasakO, LyubimovaA, KujalaP, BartfeldS, KosterJ, GeahlenJH
|
85 |
SugaH, KadoshimaT, MinaguchiM, OhgushiM, SoenM, NakanoT, TakataN, WatayaT, MugurumaK, MiyoshiH
|
86 |
TakahashiK, TanabeK, OhnukiM, NaritaM, IchisakaT, TomodaK, YamanakaS (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell131:861–872
|
87 |
TakasatoM, ErPX, ChiuHS, MaierB, BaillieGJ, FergusonC, PartonRG, WolvetangEJ, RoostMS, de SousaChuva, LopesSM (2015) Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature526:564–568
|
88 |
TakebeT, SekineK, EnomuraM, KoikeH, KimuraM, OgaeriT, ZhangRR, UenoY, ZhengYW, KoikeN
|
89 |
TakebeT, ZhangRR, KoikeH, KimuraM, YoshizawaE, EnomuraM, KoikeN, SekineK, TaniguchiH (2014) Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant. Nat Protoc9:396–409
|
90 |
ThakorePI, D’IppolitoAM, SongL, SafiA, ShivakumarNK, KabadiAM, ReddyTE, CrawfordGE, GersbachCA (2015) Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements. Nat Methods12:1143–1149
|
91 |
van de WeteringM, FranciesHE, FrancisJM, BounovaG, IorioF, PronkA, van HoudtW, van GorpJ, Taylor-WeinerA, KesterL
|
92 |
ViscontiRP, KasyanovV, GentileC, ZhangJ, MarkwaldRR, MironovV (2010) Towards organ printing: engineering an intra-organ branched vascular tree. Expert Opin Biol Ther10:409–420
|
93 |
WangF, QiLS (2016) Applications of CRISPR genome engineering in cell biology. Trends Cell Biol26:875–888
|
94 |
WangT, WeiJJ, SabatiniDM, LanderES (2014) Genetic screens in human cells using the CRISPR-Cas9 system. Science343:80–84
|
95 |
WangX, YamamotoY, WilsonLH, ZhangT, HowittBE, FarrowMA, KernF, NingG, HongY, KhorCC
|
96 |
WatsonCL, MaheMM, MúneraJ, HowellJC, SundaramN, PolingHM, SchweitzerJI, VallanceJE, MayhewCN, SunY
|
97 |
WilsonSS, TocchiA, HollyMK, ParksWC, SmithJG (2015) A small intestinal organoid model of non-invasive enteric pathogenepithelial cell interactions. Mucosal Immunol8:352–361
|
98 |
WorkmanMJ, MaheMM, TrisnoS, PolingHM, WatsonCL, SundaramN, ChangCF, SchiesserJ, AubertP, StanleyEG (2016) Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system. Nat Med. doi: 10.1038/nm.4233
|
99 |
WroblewskiLE, PiazueloMB, ChaturvediR, SchumacherM, AiharaE, FengR, NotoJM, DelgadoA, IsraelDA, ZavrosY (2015) Helicobacter pylori targets cancer-associated apical-junctional constituents in gastroids and gastric epithelial cells. Gut64:720–730
|
100 |
YinX, FarinHF, van EsJH, CleversH, LangerR, KarpJM (2014) Niche-independent high-purify cultures of Lgr5+ intestinal stem cells and their progeny. Nat Methods11:106–112
|
101 |
YinX, MeadBE, SafaeeH, LangerR, KarpJM, LevyO (2016) Engieering stem cell organoids. Cell Stem Cell18:25–38
|
102 |
YuJ, VodyanikMA, Smuga-OttoK, Antosiewicz-BourgetJ, FraneJL, TianS, NieJ, JonsdottirGA, RuottiV, StewartR
|
103 |
ZhangYG, WuS, XiaY, SunJ (2014) Salmonella-infected cryptderived intestinal organoid culture system for host-bacterial interactions. Physiol Rep2(9):e12147
|
104 |
ZhangW, LiJ, SuzukiK, QuJ, WangP, ZhouJ, LiuX, RenR, XuX, OcampoA
|
105 |
ZhouY, ZhuS, CaiC, YuanP, LiC, HuangY, WeiW (2014) Highthroughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature509:487–491
|
106 |
ZhuS, LiW, LiuJ, ChenCH, LiaoQ, XuP, XuH, XiaoT, CaoZ, PengJ
|
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|
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