Retinoic acid-mediated regulation of GLI3 enables efficient motoneuron derivation from human ESCs in the absence of extrinsic SHH activation

Journal of Neuroscience

Volumn 35, Issue 33, 2015, Pages 11462-11481

  Calder, Elizabeth L ^a,b,d   Tchieu, Jason ^a,b   Steinbeck, Julius A ^a,b   Tu, Edmund ^a,b   Keros, Sotirios ^c   Ying, Shui Wang ^c   Jaiswal, Manoj K ^c   Cornacchia, Daniela ^a,b   Goldstein, Peter A ^c   Tabar, Viviane ^a,b,d   Studer, Lorenz ^a,b,d  

^a The Center for Stem Cell Biology   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d Weill Cornell Medical Center   (United States)

Author keywords

Directed differentiation; Gli3; Motoneurons; Pluripotent stem cells; Retinoic acid; SHH signaling

Indexed keywords

GENOMIC DNA; HEPATOCYTE NUCLEAR FACTOR 3BETA; NETRIN 1; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; RETINOIC ACID; RETINOIC ACID RECEPTOR; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR LHX3; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTOME; GLI3 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; NERVE PROTEIN; SHH PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE SEQUENCE; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; MOLECULAR CLONING; MOTONEURON; MOUSE; MYOBLAST; NERVE CELL DIFFERENTIATION; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; WHOLE CELL PATCH CLAMP; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY;

CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MOTOR NEURONS; NERVE TISSUE PROTEINS; TRETINOIN;

EID: 84939838910     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3046-14.2015     Document Type: Article

References (58)

1. Abbasi AA, Paparidis Z, Malik S, Goode DK, Callaway H, Elgar G, Grzeschik KH (2007) Human GLI3 intragenic conserved non-coding sequences are tissue-specific enhancers. PLoS One 2:e366. CrossRef Medline
2. Abbasi AA, Paparidis Z, Malik S, Bangs F, Schmidt A, Koch S, Lopez-Rios J, Grzeschik KH (2010) Human intronic enhancers control distinct subdomains of Gli3 expression during mouse CNS and limb development. BMC Dev Biol 10:44. CrossRef Medline
3. Ahn S, Joyner AL (2004) Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118:505-516. CrossRef Medline
4. Amoroso MW, Croft GF, Williams DJ, O'Keeffe S, Carrasco MA, Davis AR, Roybon L, Oakley DH, Maniatis T, Henderson CE, Wichterle H (2013) Accelerated high-yield generation of limb-innervating motor neurons from human stem cells. J Neurosci 33:574 -586. CrossRef Medline
5. Bai CB, Stephen D, Joyner AL (2004) All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev Cell 6:103-115. CrossRef Medline
6. Barreto-Chang OL, Dolmetsch RE (2009) Calcium imaging of cortical neurons using Fura-2 AM. J Vis Exp pii:1067. CrossRef Medline
7. Boulting GL, Kiskinis E, Croft GF, Amoroso MW, Oakley DH, Wainger BJ, Williams DJ, Kahler DJ, Yamaki M, Davidow L, Rodolfa CT, Dimos JT, Mikkilineni S, MacDermott AB, Woolf CJ, Henderson CE, Wichterle H, Eggan K (2011) A functionally characterized test set of human induced pluripotent stem cells. Nat Biotechnol 29:279 -286. CrossRef Medline
8. Briscoe J, Pierani A, Jessell TM, Ericson J (2000) A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101:435- 445. CrossRef Medline
9. Bynum SV (1991) Morphogenesis of retinoic acid-induced postaxial polydactyly in mice. Teratology 43:1-9. CrossRef Medline
10. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27:275-280. CrossRef Medline
11. Chambers SM, Qi Y, Mica Y, Lee G, Zhang XJ, Niu L, Bilsland J, Cao L, Stevens E, Whiting P, Shi SH, Studer L (2012) Combined smallmolecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nat Biotechnol 30:715-720. CrossRef Medline
12. Coy S, Caaman˜o JH, Carvajal J, Cleary ML, Borycki AG (2011) A novel Gli3 enhancer controls the Gli3 spatiotemporal expression pattern through a TALE homeodomain protein binding site. Mol Cell Biol 31:1432-1443. CrossRef Medline
13. Dasen JS, Liu JP, JessellTM (2003) Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425:926 -933. CrossRef Medline
14. Dasen JS, Tice BC, Brenner-Morton S, Jessell TM (2005) A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123:477- 491. CrossRef Medline
15. Davis-Dusenbery BN, Williams LA, Klim JR, Eggan K (2014) How to make spinal motor neurons. Development 141:491-501. CrossRef Medline
16. Dessaud E, Yang LL, Hill K, Cox B, Ulloa F, Ribeiro A, Mynett A, Novitch BG, Briscoe J (2007) Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450:717-720. CrossRef Medline
17. Dessaud E, McMahon AP, Briscoe J (2008) Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135:2489 -2503. CrossRef Medline
18. Dow LE, Premsrirut PK, Zuber J, Fellmann C, McJunkin K, Miething C, Park Y, Dickins RA, Hannon GJ, Lowe SW (2012) A pipeline for the generation of shRNA transgenic mice. Nat Protoc 7:374 -393. CrossRef Medline
19. Ericson J, Morton S, Kawakami A, Roelink H, JessellTM (1996) Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87:661- 673. CrossRef Medline
20. Fasano CA, Chambers SM, Lee G, Tomishima MJ, Studer L (2010) Efficient derivation of functional floor plate tissue from human embryonic stem cells. Cell Stem Cell 6:336 -347. CrossRef Medline
21. Fawcett D, Pasceri P, Fraser R, Colbert M, Rossant J, Gigue`re V (1995) Postaxial polydactyly in forelimbs of CRABP-II mutant mice. Development 121:671- 679. Medline
22. Harper JM, Krishnan C, Darman JS, DeshpandeDM,Peck S, Shats I, Backovic S, Rothstein JD, Kerr DA (2004) Axonal growth of embryonic stem cellderived motoneurons in vitro and in motoneuron-injured adult rats. Proc Natl Acad Sci U S A 101:7123-7128. CrossRef Medline
23. Hasenpusch-Theil K, Magnani D, Amaniti EM, Han L, Armstrong D, Theil T (2012) Transcriptional analysis of Gli3 mutants identifies Wnt target genes in the developing hippocampus. Cereb Cortex 22:2878 -2893. CrossRef Medline
24. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38:576 -589. CrossRef Medline
25. Hill P, Go¨tz K, Ru¨ther U (2009) A SHH-independent regulation of Gli3 is a significant determinant of anteroposterior patterning of the limb bud. Dev Biol 328:506 -516. CrossRef Medline
26. Hu BY, Zhang SC (2009) Differentiation of spinal motor neurons from pluripotent human stem cells. Nat Protoc 4:1295-1304. CrossRef Medline
27. Hui CC, Joyner AL (1993) A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat Genet 3:241-246. CrossRef Medline
28. Kriks S, Shim JW, Piao J, Ganat YM, Wakeman DR, Xie Z, Carrillo-Reid L, Auyeung G, Antonacci C, Buch A, Yang L, Beal MF, Surmeier DJ, Kordower JH, Tabar V, Studer L (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480:547-551. Medline
29. Lee H, Shamy GA, Elkabetz Y, Schofield CM, Harrsion NL, Panagiotakos G, Socci ND, Tabar V, Studer L (2007) Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons. Stem Cells 25:1931-1939. CrossRef Medline
30. Lei Q, Zelman AK, Kuang E, Li S, MatiseMP (2004) Transduction of graded Hedgehog signaling by a combination of Gli2 and Gli3 activator functions in the developing spinal cord. Development 131:3593-3604. CrossRef Medline
31. Li XJ, Du ZW, Zarnowska ED, Pankratz M, Hansen LO, Pearce RA, Zhang SC (2005) Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 23:215-221. CrossRef Medline
32. Li XJ, Hu BY, Jones SA, Zhang YS, Lavaute T, Du ZW, Zhang SC (2008) Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells 26:886- 893. CrossRef Medline
33. Litingtung Y, Chiang C (2000) Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat Neurosci 3:979 -985. CrossRef Medline
34. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823- 826. CrossRef Medline
35. Mazzoni EO, Mahony S, Closser M, Morrison CA, Nedelec S, Williams DJ, An D, Gifford DK, Wichterle H (2013a) Synergistic binding of transcription factors to cell-specific enhancers programs motor neuron identity. Nat Neurosci 16:1219 -1227. CrossRef Medline
36. Mazzoni EO, Mahony S, Peljto M, Patel T, Thornton SR, McCuine S, Reeder C, Boyer LA, Young RA, Gifford DK, Wichterle H (2013b) Saltatory remodeling of Hox chromatin in response to rostrocaudal patterning signals. Nat Neurosci 16:1191-1198. CrossRef Medline
37. Miles GB, Yohn DC, Wichterle H, Jessell TM, Rafuse VF, Brownstone RM (2004) Functional properties of motoneurons derived from mouse embryonic stem cells. J Neurosci 24:7848 -7858. CrossRef Medline
38. Ogura T, Alvarez IS, Vogel A, Rodríguez C, Evans RM, Izpisu´ a Belmonte JC (1996) Evidence that Shh cooperates with a retinoic acid inducible cofactor to establish ZPA-like activity. Development 122:537-542. Medline
39. Patani R, Hollins AJ, Wishart TM, Puddifoot CA, Alvarez S, de Lera AR, Wyllie DJ, Compston DA, Pedersen RA, Gillingwater TH, Hardingham GE, Allen ND, Chandran S (2011) Retinoid-independent motor neurogenesis from human embryonic stem cells reveals a medial columnar ground state. Nat Commun 2:214. CrossRef Medline
40. Peljto M, Dasen JS, Mazzoni EO, Jessell TM, WichterleH (2010) Functional diversity of ESC-derived motor neuron subtypes revealed through intraspinal transplantation. Cell Stem Cell 7:355-366. CrossRef Medline
41. Persson M, Stamataki D, te Welscher P, Andersson E, Bo¨se J, Ru¨ther U, Ericson J, Briscoe J (2002) Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev 16:2865-2878. CrossRef Medline
42. Placantonakis DG, Tomishima MJ, Lafaille F, Desbordes SC, Jia F, Socci ND, Viale A, Lee H, Harrison N, Tabar V, Studer L (2009) BAC transgenesis in human embryonic stem cells as a novel tool to define the human neural lineage. Stem Cells 27:521-532. CrossRef Medline
43. Qu Q, Li D, Louis KR, Li X, Yang H, Sun Q, Crandall SR, Tsang S, Zhou J, Cox CL, Cheng J, Wang F (2014) High-efficiency motor neuron differentia- tion from human pluripotent stem cells and the function of Islet-1. Nat Commun 5:3449. Medline
44. Rallu M, Machold R, Gaiano N, Corbin JG, McMahon AP, Fishell G (2002) Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and Hedgehog signaling. Development 129:4963- 4974. Medline
45. Renoncourt Y, Carroll P, Filippi P, Arce V, Alonso S (1998) Neurons derived in vitro from ES cells express homeoproteins characteristic of motoneurons and interneurons. Mech Dev 79:185-197. CrossRef Medline
46. Ruiz i Altaba A (1998) Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development 125:2203-2212. Medline
47. Singh Roy N, Nakano T, Xuing L, Kang J, Nedergaard M, Goldman SA (2005) Enhancer-specified GFP-based FACS purification of human spinal motor neurons from embryonic stem cells. Exp Neurol 196:224 -234. CrossRef Medline
48. Son EY, Ichida JK, Wainger BJ, Toma JS, Rafuse VF, Woolf CJ, Eggan K (2011) Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell 9:205-218. CrossRef Medline
49. Soundararajan P, Miles GB, Rubin LL, Brownstone RM, Rafuse VF (2006) Motoneurons derived from embryonic stem cells express transcription factors and develop phenotypes characteristic of medial motor column neurons. J Neurosci 26:3256 -3268. CrossRef Medline
50. Takazawa T, Croft GF, Amoroso MW, Studer L, Wichterle H, Macdermott AB (2012) Maturation of spinal motor neurons derived from human embryonic stem cells. PLoS One 7:e40154. CrossRef Medline
51. Umbach JA, Adams KL, Gundersen CB, Novitch BG (2012) Functional neuromuscular junctions formed by embryonic stem cell-derived motor neurons. PLoS One 7:e36049. CrossRef Medline
52. Wang B, Fallon JF, Beachy PA (2000) Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100:423- 434. CrossRef Medline
53. Wang H, Meyer CA, Fei T, Wang G, Zhang F, Liu XS (2013) A systematic approach identifies FOXA1 as a key factor in the loss of epithelial traits during the epithelial-to-mesenchymal transition in lung cancer. BMC Genomics 14:680. CrossRef Medline
54. Wichterle H, Lieberam I, Porter JA, Jessell TM (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385-397. CrossRef Medline
55. Wijgerde M, McMahon JA, Rule M, McMahon AP (2002) A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev 16:2849 -2864. CrossRef Medline
56. Xie W, Schultz MD, Lister R, Hou Z, Rajagopal N, Ray P, Whitaker JW, Tian S, Hawkins RD, Leung D, Yang H, Wang T, Lee AY, Swanson SA, Zhang J, Zhu Y, Kim A, Nery JR, Urich MA, Kuan S, et al. (2013) Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153:1134 -1148. CrossRef Medline
57. Ying SW, Goldstein PA (2005) Propofol-block of SK channels in reticular thalamic neurons enhances GABAergic inhibition in relay neurons. J Neurophysiol 93:1935-1948. Medline
58. Ying SW, Jia F, Abbas SY, Hofmann F, Ludwig A, Goldstein PA (2007) Dendritic HCN2 channels constrain glutamate-driven excitability in reticular thalamic neurons. J Neurosci 27:8719-8732. CrossRef Medline