Modelling and rescuing neurodevelopmental defect of Down syndrome using induced pluripotent stem cells from monozygotic twins discordant for trisomy 21

EMBO Molecular Medicine

Volumn 6, Issue 2, 2014, Pages 259-277

  Hibaoui, Youssef ^a,b   Grad, Iwona ^a   Letourneau, Audrey ^b   Sailani, M Reza ^b   Dahoun, Sophie ^b   Santoni, Federico A ^b   Gimelli, Stefania ^b   Guipponi, Michel ^b   Pelte, Marie Françoise ^c   Béna, Frédérique ^b   Antonarakis, Stylianos E ^b,c   Feki, Anis ^a,d  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d Hopital Cantonal de Fribourg   (Switzerland)

Author keywords

Disease modelling; Down syndrome; DYRK1A; Induced pluripotent stem cells; Neurodevelopment

Indexed keywords

ALKALINE PHOSPHATASE; ALPHA FETOPROTEIN; ALPHA SMOOTH MUSCLE ACTIN; BETA TUBULIN; GLUTAMATE DECARBOXYLASE 67; KRUPPEL LIKE FACTOR 4; MICROTUBULE ASSOCIATED PROTEIN 2; OCTAMER TRANSCRIPTION FACTOR 4; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN S100B; SHORT HAIRPIN RNA; STAGE SPECIFIC EMBRYO ANTIGEN 4; SYNAPSIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; VIMENTIN; ZINC FINGER PROTEIN;

APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; CELL DENSITY; CHROMOSOME 21; COMPARATIVE GENOMIC HYBRIDIZATION; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN SYNDROME; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; KARYOTYPE; MACROGLIA; MONOZYGOTIC TWINS; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; OLIGODENDROGLIA; ONCOGENE C MYC; ORGANOGENESIS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; RNA SEQUENCE; TERATOMA; TRISOMY 21; TWIN DISCORDANCE;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; DOWN SYNDROME; GENE ONTOLOGY; GENOME, HUMAN; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, INBRED NOD; MICE, SCID; MODELS, BIOLOGICAL; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; TRANSCRIPTOME; TWINS, MONOZYGOTIC;

EID: 84893772144     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201302848     Document Type: Article

References (73)

1. Ables JL, Breunig JJ, Eisch AJ, Rakic P (2011) Not(ch) just development: Notch signalling in the adult brain. Nat Rev Neurosci 12: 269-283
2. Abrajano JJ, Qureshi IA, Gokhan S, Zheng D, Bergman A, Mehler MF (2009) REST and CoREST modulate neuronal subtype specification, maturation and maintenance. PLoS One 4: e7936
3. Ahn K-J, Jeong HK, Choi H-S, Ryoo S-R, Kim YJ, Goo J-S, Choi S-Y, Han J-S, Ha I, Song W-J (2006) DYRK1A BAC transgenic mice show altered synaptic plasticity with learning and memory defects. Neurobiol Dis 22: 463-472
4. Altafaj X, Dierssen M, Baamonde C, Martí E, Visa J, Guimerà J, Oset M, González JR, Flórez J, Fillat C et al (2001) Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum Mol Genet 10: 1915-1923
5. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106
6. Antonarakis SE, Lyle R, Dermitzakis ET, Reymond A, Deutsch S (2004) Chromosome 21 and Down syndrome: from genomics to pathophysiology. Nat Rev Genet 5: 725-738
7. Bahn S, Mimmack M, Ryan M, Caldwell M, Jauniaux E, Starkey M, Svendsen C, Emson P (2002) Neuronal target genes of the neuron-restrictive silencer factor in neurospheres derived from fetuses with Down's syndrome: a gene expression study. Lancet 359: 310-315
8. Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G (2005) REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121: 645-657
9. Becker L, Mito T, Takashima S, Onodera K (1991) Growth and development of the brain in Down syndrome. Prog Clin Biol Res 373: 133-152
10. Becker W, Weber Y, Wetzel K, Eirmbter K, Tejedor FJ, Joost H-G (1998) Sequence characteristics, subcellular localization, and substrate specificity of DYRK-related kinases, a novel family of dual specificity protein kinases. J Biol Chem 273: 25893-25902
11. Belichenko PV, Kleschevnikov AM, Salehi A, Epstein CJ, Mobley WC (2007) Synaptic and cognitive abnormalities in mouse models of down syndrome: exploring genotype-phenotype relationships. J Comp Neurol 504: 329-345
12. Benavides-Piccione R, Dierssen M, Ballesteros-Yáñez I, Martínez de Lagrán M, Arbonés ML, Fotaki V, DeFelipe J, Elston GN (2005) Alterations in the phenotype of neocortical pyramidal cells in the Dyrk1A+/- mouse. Neurobiol Dis 20: 115-122
13. Bhattacharyya A, McMillan E, Chen SI, Wallace K, Svendsen CN (2009) A critical period in cortical interneuron neurogenesis in Down syndrome revealed by human neural progenitor cells. Dev Neurosci 31: 497-510
14. Biancotti J-C, Narwani K, Buehler N, Mandefro B, Golan-Lev T, Yanuka O, Clark A, Hill D, Benvenisty N, Lavon N (2010) Human embryonic stem cells as models for aneuploid chromosomal syndromes. Stem Cells 28: 1530-1540
15. Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S, Li Y, Mu Y, Chen G, Yu D et al (2011) Modelling schizophrenia using human induced pluripotent stem cells. Nature 473: 221-225
16. Breunig JJ, Silbereis J, Vaccarino FM, Šestan N, Rakic P (2007) Notch regulates cell fate and dendrite morphology of newborn neurons in the postnatal dentate gyrus. Proc Natl Acad Sci USA 104: 20558-20563
17. Canzonetta C, Mulligan C, Deutsch S, Ruf S, O'Doherty A, Lyle R, Borel C, Lin-Marq N, Delom F, Groet J et al (2008) DYRK1A-dosage imbalance perturbs NRSF/REST evels, deregulating pluripotency and embryonic stem cell fate in Down Syndrome. Am J Hum Genet 83: 388-400
18. Chakrabarti L, Galdzicki Z, Haydar TF (2007) Defects in embryonic neurogenesis and initial synapse formation in the forebrain of the Ts65Dn mouse model of Down syndrome. J Neurosci 27: 11483-11495
19. Ciani L, Salinas PC (2005) WNTS in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 6: 351-362
20. Contestabile A, Fila T, Ceccarelli C, Bonasoni P, Bonapace L, Santini D, Bartesaghi R, Ciani E (2007) Cell cycle alteration and decreased cell proliferation in the hippocampal dentate gyrus and in the neocortical germinal matrix of fetuses with down syndrome and in Ts65Dn mice. Hippocampus 17: 665-678
21. Dahoun S, Gagos S, Gagnebin M, Gehrig C, Burgi C, Simon F, Vieux C, Extermann P, Lyle R, Morris MA et al (2008) Monozygotic twins discordant for trisomy 21 and maternal 21q inheritance: a complex series of events. Am J Med Genet 146A: 2086-2093
22. Das I, Reeves RH (2011) The use of mouse models to understand and improve cognitive deficits in Down syndrome. Dis Model Mech 4: 596-606
23. Dierssen M, Benavides-Piccione R, Martínez-Cué C, Estivill X, Flórez J, Elston GN, DeFelipe J (2003) Alterations of neocortical pyramidal cell phenotype in the Ts65Dn mouse model of Down syndrome: effects of environmental enrichment. Cereb Cortex 13: 758-764
24. Esposito G, Imitola J, Lu J, De Filippis D, Scuderi C, Ganesh VS, Folkerth R, Hecht J, Shin S, Iuvone T et al (2008) Genomic and functional profiling of human Down syndrome neural progenitors implicates S100B and aquaporin 4 in cell injury. Hum Mol Genet 17: 440-457
25. Fotaki V, Dierssen M, Alcántara S, Martínez S, Martí E, Casas C, Visa J, Soriano E, Estivill X, Arbonés ML (2002) Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice. Mol Cell Biol 22: 6636-6647
26. Freberg CT, Dahl JA, Timoskainen S, Collas P (2007) Epigenetic reprogramming of OCT4 and NANOG regulatory regions by embryonal carcinoma cell extract. Mol Biol Cell 18: 1543-1553
27. Grad I, Hibaoui Y, Jaconi M, Chicha L, Bergström-Tengzelius R, Sailani MR, Pelte MF, Dahoun S, Mitsiadis TA, Töhönen V et al (2011) NANOG priming before full reprogramming may generate germ cell tumours. Eur Cell Mater 22: 258-274
28. Guedj F, Sébrié C, Rivals I, Ledru A, Paly E, Bizot JC, Smith D, Rubin E, Gillet B, Arbones M et al (2009) Green tea polyphenols rescue of brain defects induced by overexpression of DYRK1A. PLoS One 4: e4606
29. Guidi S, Bonasoni P, Ceccarelli C, Santini D, Gualtieri F, Ciani E, Bartesaghi R (2008) Neurogenesis impairment and increased cell death reduce total neuron number in the hippocampal region of fetuses with Down syndrome. Brain Pathol 18: 180-197
30. Guidi S, Ciani E, Bonasoni P, Santini D, Bartesaghi R (2011) Widespread proliferation impairment and hypocellularity in the cerebellum of fetuses with Down syndrome. Brain Pathol 21: 361-373
31. Guimera J, Casas C, Pucharcôs C, Solans A, Domènech A, Planas AM, Ashley J, Lovett M, Estivill X, Pritchard MA (1996) A human homologue of drosophila minibrain (Mnb) is expressed in the neuronal regions affected in Down syndrome and maps to the critical region. Hum Mol Genet 5: 1305-1310
32. Hämmerle B, Ulin E, Guimera J, Becker W, Guillemot F, Tejedor FJ (2011) Transient expression of Mnb/Dyrk1a couples cell cycle exit and differentiation of neuronal precursors by inducing p27KIP1 expression and suppressing NOTCH signaling. Development 138: 2543-2554
33. Hibaoui Y, Feki A (2012) Human pluripotent stem cells: applications and challenges in neurological diseases. Front Physiol 3: 267
34. Hibaoui Y, Roulet E, Ruegg UT (2009) Melatonin prevents oxidative stress-mediated mitochondrial permeability transition and death in skeletal muscle cells. J Pineal Res 47: 238-252
35. Huang DW, Sherman BT, Lempicki RA (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
36. Huang DW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13
37. Israel MA, Yuan SH, Bardy C, Reyna SM, Mu Y, Herrera C, Hefferan MP, Van Gorp S, Nazor KL, Boscolo FS et al (2012) Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482: 216-20
38. Kleschevnikov AM, Belichenko PV, Villar AJ, Epstein CJ, Malenka RC, Mobley WC (2004) Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J Neurosci 24: 8153-8160
39. Korbel JO, Tirosh-Wagner T, Urban AE, Chen X-N, Kasowski M, Dai L, Grubert F, Erdman C, Gao MC, Lange K et al (2009) The genetic architecture of Down syndrome phenotypes revealed by high-resolution analysis of human segmental trisomies. Proc Natl Acad Sci USA 106: 12031-12036
40. Kuwabara T, Hsieh J, Nakashima K, Taira K, Gage FH (2004) A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 116: 779-793
41. Laguna A, Aranda S, Barallobre MJ, Barhoum R, Fernández E, Fotaki V, Delabar JM, de la Luna S, de la Villa P, Arbonés ML (2008) The protein kinase DYRK1A regulates caspase-9-mediated apoptosis during retina development. Dev Cell 15: 841-853
42. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760
43. Lilienthal E, Kolanowski K, Becker W (2010) Development of a sensitive non-radioactive protein kinase assay and its application for detecting DYRK activity in Xenopus laevis oocytes. BMC Biochem 11: 20
44. Litovchick L, Florens LA, Swanson SK, Washburn MP, DeCaprio JA (2011) DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly. Genes Dev 25: 801-813
45. Lott IT, Dierssen M (2010) Cognitive deficits and associated neurological complications in individuals with Down's syndrome. Lancet Neurol 9: 623-633
46. Lu J, Esposito G, Scuderi C, Steardo L, Delli-Bovi LC, Hecht JL, Dickinson BC, Chang CJ, Mori T, Sheen V (2011) S100B and APP promote a gliocentric shift and impaired neurogenesis in Down syndrome neural progenitors. PLoS One 6: e2212
47. Lu J, Lian G, Zhou H, Esposito G, Steardo L, Delli-Bovi LC, Hecht JL, Lu QR, Sheen V (2012) OLIG2 over-expression impairs proliferation of human Down syndrome neural progenitors. Hum Mol Genet 21: 2330-2340
48. Lyle R, Bena F, Gagos S, Gehrig C, Lopez G, Schinzel A, Lespinasse J, Bottani A, Dahoun S, Taine L et al (2008) Genotype-phenotype correlations in Down syndrome identified by array CGH in 30 cases of partial trisomy and partial monosomy chromosome 21. Eur J Hum Genet 17: 454-466
49. Martinez de Lagran M, Benavides-Piccione R, Ballesteros-Yañez I, Calvo M, Morales M, Fillat C, DeFelipe J, Ramakers GJA, Dierssen M (2012) Dyrk1A influences neuronal morphogenesis through regulation of cytoskeletal dynamics in mammalian cortical neurons. Cereb Cortex 22: 2867-77
50. Martínez-Cué C, Martínez P, Rueda N, Vidal R, García S, Vidal V, Corrales A, Montero JA, Pazos Á, Flórez J et al (2013) Reducing GABAA α5 receptor-mediated inhibition rescues functional and neuromorphological deficits in a mouse model of down syndrome. J Neurosci 33: 3953-3966
51. Mazur-Kolecka B, Golabek A, Kida E, Rabe A, Hwang Y-W, Adayev T, Wegiel J, Flory M, Kaczmarski W, Marchi E et al (2012) Effect of DYRK1A activity inhibition on development of neuronal progenitors isolated from Ts65Dn mice. J Neurosci Res 90: 999-1010
52. Mensah A, Mulligan C, Linehan J, Ruf S, O'Doherty A, Grygalewicz B, Shipley J, Groet J, Tybulewicz V, Fisher E et al (2007) An additional human chromosome 21 causes suppression of neural fate of pluripotent mouse embryonic stem cells in a teratoma model. BMC Dev Biol 7: 131
53. Mito T, Becker LE (1993) Developmental changes of S-100 protein and glial fibrillary acidic protein in the brain in Down syndrome. Exp Neurol 120: 170-176
54. Møller RS, Kübart S, Hoeltzenbein M, Heye B, Vogel I, Hansen CP, Menzel C, Ullmann R, Tommerup N, Ropers H-H et al (2008) Truncation of the Down syndrome candidate gene DYRK1A in two unrelated patients with microcephaly. Am J Hum Genet 82: 1165-1170
55. de la Monte SM, Sohn YK, Ganju N, Wands JR (1998) P53- and CD95-associated apoptosis in neurodegenerative diseases. Lab Invest 78: 401-411
56. Park I-H, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, Cowan C, Hochedlinger K, Daley GQ (2008) Disease-specific induced pluripotent stem cells. Cell 134: 877-886
57. Park J, Oh Y, Yoo L, Jung M-S, Song W-J, Lee S-H, Seo H, Chung KC (2010) Dyrk1A phosphorylates p53 and inhibits proliferation of embryonic neuronal cells. J Biol Chem 285: 31895-31906
58. Peirson SN, Butler JN, Foster RG (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res 31: e73
59. Robinson MD, McCarthy DJ, Smyth GK (2010) EdgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140
60. Seidl R, Fang-Kircher S, Bidmon B, Cairns N, Lubec G (1999) Apoptosis-associated proteins p53 and APO-1/Fas (CD95) in brains of adult patients with Down syndrome. Neurosci Lett 260: 9-12
61. Shi Y, Kirwan P, Smith J, MacLean G, Orkin SH, Livesey FJ (2012) A human stem cell model of early Alzheimer's disease pathology in Down syndrome. Sci Transl Med 4: 124ra129
62. Smith DJ, Stevens ME, Sudanagunta SP, Bronson RT, Makhinson M, Watabe AM, O'Dell TJ, Fung J, Weier HU, Cheng JF et al (1997) Functional screening of 2 Mb of human chromosome 21q22.2 in transgenic mice implicates minibrain in learning defects associated with Down syndrome. Nat Genet 16: 28-36
63. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, Hargus G, Blak A, Cooper O, Mitalipova M et al (2009) Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136: 964-977
64. Song W-J, Sternberg LR, Kasten-Sportès C, Keuren MLV, Chung S-H, Slack AC, Miller DE, Glover TW, Chiang P-W, Lou L et al (1996) Isolation of human and murine homologues of the drosophila minibrain gene: human homologue maps to 21q22.2 in the Down syndrome "critical region". Genomics 38: 331-339
65. Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6: e21800
66. Suter DM, Preynat-Seauve O, Tirefort D, Feki A, Krause KH (2009) Phenazopyridine induces and synchronizes neuronal differentaition of embryonic stem cells. J Cell Mol Med 13: 3517-3527
67. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872
68. Tejedor F, Zhu XR, Kaltenbach E, Ackermann A, Baumann A, Canal I, Heisenberg M, Fischbach KF, Pongs O (1995) minibrain: a new protein kinase family involved in postembryonic neurogenesis in Drosophila. Neuron 14: 287-301
69. Tejedor FJ, Hämmerle B (2011) MNB/DYRK1A as a multiple regulator of neuronal development. FEBS J 278: 223-235
70. Yabut O, Domogauer J, D'Arcangelo G (2010) Dyrk1A overexpression inhibits proliferation and induces premature neuronal differentiation of neural progenitor cells. J Neurosci 30: 4004-4014
71. Yamamoto T, Shimojima K, Nishizawa T, Matsuo M, Ito M, Imai K (2011) Clinical manifestations of the deletion of Down syndrome critical region including DYRK1A and KCNJ6. Am J Med Genet A 155: 113-119
72. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, Thomson JA (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324: 797-801
73. Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109: 61-73