Using human pluripotent stem cells to study post-transcriptional mechanisms of neurodegenerative diseases

Brain Research

Volumn 1462, Issue , 2012, Pages 129-138

  Patani, Rickie ^a,b,d   Sibley, Christopher R ^d   Chandran, Siddharthan ^c   Ule, Jernej ^d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Embryonic stem cell (ESC); Induced pluripotent stem cell (iPSC); Neurodegenerative disease; Pluripotent stem cell (hPSC); RNA binding protein (RBP)

Indexed keywords

LOXAPINE; RNA; RNA BINDING PROTEIN;

ARTICLE; CELL RENEWAL; DEGENERATIVE DISEASE; DISEASE MODEL; EMBRYONIC STEM CELL; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA PROCESSING; RNA SEQUENCE; SCHIZOPHRENIA;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; PLURIPOTENT STEM CELLS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA; RNA-BINDING PROTEINS; SPECIES SPECIFICITY; STEM CELLS;

EID: 84862147240     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.12.057     Document Type: Article

References (124)

1. R. Abujarour, and S. Ding Induced pluripotent stem cells free of exogenous reprogramming factors Genome Biol. 10 5 2009 220
2. G. Amabile, and A. Meissner Induced pluripotent stem cells: current progress and potential for regenerative medicine Trends Mol. Med. 15 2 2009 59 68
3. M. Amit, and V. Margulets Human feeder layers for human embryonic stem cells Biol. Reprod. 68 6 2003 2150 2156 (Pubitemid 36687007)
4. M. Amit, and C. Shariki Feeder layer- and serum-free culture of human embryonic stem cells Biol. Reprod. 70 3 2004 837 845 (Pubitemid 38233724)
5. K. Anthony, and J.M. Gallo Aberrant RNA processing events in neurological disorders Brain Res. 1338 2010 67 77
6. S. Bachurin, E. Bukatina, N. Lermontova, S. Tkachenko, A. Afanasiev, V. Grigoriev, I. Grigorieva, Y. Ivanov, S. Sablin, and N. Zefirov Antihistamine agent Dimebon as a novel neuroprotector and a cognition enhancer Ann. N. Y. Acad. Sci. 939 2001 425 435 (Pubitemid 32620096)
7. M.G. Besselink, and H.C. van Santvoort Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial Lancet 371 9613 2008 651 659
8. I. Bezprozvanny The rise and fall of Dimebon Drug News Perspect. 23 8 2010 518 523
9. A. Bjorklund, and S.B. Dunnett Dopamine neuron systems in the brain: an update Trends Neurosci. 30 5 2007 194 202 (Pubitemid 46654237)
10. C. Bock, and E. Kiskinis Reference Maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines Cell 144 3 2011 439 452
11. G.A. Bortoff, and P.L. Strick Corticospinal terminations in two new-world primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity J. Neurosci. 13 12 1993 5105 5118 (Pubitemid 24000997)
12. P.L. Boutz, P. Stoilov, Q. Li, C.H. Lin, G. Chawla, K. Ostrow, L. Shiue, M. Ares Jr., and D.L. Black A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons Genes Dev. 21 13 2007 1636 1652 (Pubitemid 47026368)
13. K.J. Brennand, and A. Simone Modelling schizophrenia using human induced pluripotent stem cells Nature 473 7346 2011 221 225
14. K.H. Campbell, and J. McWhir Sheep cloned by nuclear transfer from a cultured cell line Nature 380 6569 1996 64 66 (Pubitemid 26076237)
15. L. Cartegni, and M.L. Hastings Determinants of exon 7 splicing in the spinal muscular atrophy genes, SMN1 and SMN2 Am. J. Hum. Genet. 78 1 2006 63 77 (Pubitemid 41833160)
16. T. Cathomen, and A. Schambach Zinc-finger nucleases meet iPS cells: zinc positive: tailored genome engineering meets reprogramming Gene Ther. 17 1 2010 1 3
17. S.M. Chambers, and C.A. Fasano Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling Nat. Biotechnol. 27 3 2009 275 280
18. M.H. Chin, and M.J. Mason Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures Cell Stem Cell 5 1 2009 111 123
19. S. Chung, B.S. Shin, E. Hedlund, J. Pruszak, A. Ferree, U.J. Kang, O. Isacson, and K.S. Kim Genetic selection of sox1GFP-expressing neural precursors removes residual tumorigenic pluripotent stem cells and attenuates tumor formation after transplantation J. Neurochem. 97 5 2006 1467 1480 (Pubitemid 43725585)
20. G. Courtine, and R.R. Roy Performance of locomotion and foot grasping following a unilateral thoracic corticospinal tract lesion in monkeys (Macaca mulatta) Brain 128 Pt 10 2005 2338 2358 (Pubitemid 41407974)
21. G. Courtine, and M.B. Bunge Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans? Nat. Med. 13 5 2007 561 566 (Pubitemid 46828491)
22. C.A. Cowan, and J. Atienza Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells Science 309 5739 2005 1369 1373 (Pubitemid 41209363)
23. A. Dahlstrom, and K. Fuxe Localization of monoamines in the lower brain stem Experientia 20 7 1964 398 399
24. M. Dejesus-Hernandez, and I.R. Mackenzie Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS Neuron 72 2 2011 245 256
25. E.T. Dermitzakis, and A.G. Clark Evolution of transcription factor binding sites in Mammalian gene regulatory regions: conservation and turnover Mol. Biol. Evol. 19 7 2002 1114 1121 (Pubitemid 34743235)
26. F.P. Di Giorgio, and M.A. Carrasco Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model Nat. Neurosci. 10 5 2007 608 614 (Pubitemid 46652442)
27. F.P. Di Giorgio, and G.L. Boulting Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation Cell Stem Cell 3 6 2008 637 648
28. M.T. Dirksen, and G.J. Laarman Reperfusion injury in humans: a review of clinical trials on reperfusion injury inhibitory strategies Cardiovasc. Res. 74 3 2007 343 355 (Pubitemid 46693697)
29. A. Disset, and C.F. Bourgeois An exon skipping-associated nonsense mutation in the dystrophin gene uncovers a complex interplay between multiple antagonistic splicing elements Hum. Mol. Genet. 15 6 2006 999 1013 (Pubitemid 43338240)
30. A.D. Ebert, and J. Yu Induced pluripotent stem cells from a spinal muscular atrophy patient Nature 457 7227 2009 277 280
31. M. Eiraku, and K. Watanabe Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals Cell Stem Cell 3 5 2008 519 532
32. A. Eisen Amyotrophic lateral sclerosis-Evolutionary and other perspectives Muscle Nerve 40 2 2009 297 304
33. M.J. Evans, and M.H. Kaufman Establishment in culture of pluripotential cells from mouse embryos Nature 292 5819 1981 154 156 (Pubitemid 11050741)
34. P. Freund, and E. Schmidlin Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates Nat. Med. 12 7 2006 790 792 (Pubitemid 44050068)
35. T. Frugier, and F.D. Tiziano Nuclear targeting defect of SMN lacking the C-terminus in a mouse model of spinal muscular atrophy Hum. Mol. Genet. 9 5 2000 849 858 (Pubitemid 30162771)
36. F. Gonzalez, and S. Boue Methods for making induced pluripotent stem cells: reprogramming a la carte Nat. Rev. Genet. 12 4 2011 231 242
37. J.B. Gurdon, and T.R. Elsdale Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei Nature 182 4627 1958 64 65
38. S.S. Han, and L.A. Williams Constructing and deconstructing stem cell models of neurological disease Neuron 70 4 2011 626 644
39. G.E. Hardingham, and R. Patani Human embryonic stem cell-derived neurons as a tool for studying neuroprotection and neurodegeneration Mol. Neurobiol. 42 1 2010 97 102
40. B.Y. Hu, and J.P. Weick Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency Proc. Natl. Acad. Sci. U. S. A. 107 9 2010 4335 4340
41. F. Jia, K.D. Wilson, N. Sun, D.M. Gupta, M. Huang, Z. Li, N.J. Panetta, Z.Y. Chen, R.C. Robbins, M.A. Kay, M.T. Longaker, and J.C. Wu A nonviral minicircle vector for deriving human iPS cells Nat. Methods 7 3 2010 197 199
42. P. Jin, and R. Duan Pur alpha binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a Drosophila model of fragile X tremor/ataxia syndrome Neuron 55 4 2007 556 564 (Pubitemid 47223639)
43. A.J. Joannides, and C. Fiore-Heriche A scaleable and defined system for generating neural stem cells from human embryonic stem cells Stem Cells 25 3 2007 731 737 (Pubitemid 46354233)
44. J. Konig, and K. Zarnack iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution Nat. Struct. Mol. Biol. 17 7 2010 909 915
45. R. Krencik, and J.P. Weick Specification of transplantable astroglial subtypes from human pluripotent stem cells Nat. Biotechnol. 29 6 2011 528 534
46. H.G. Kuypers The descending pathways to the spinal cord, their anatomy and function Prog. Brain Res. 11 1964 178 202
47. D.G. Lawrence, and H.G. Kuypers The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions Brain 91 1 1968 1 14
48. D.G. Lawrence, and H.G. Kuypers The functional organization of the motor system in the monkey. II. The effects of lesions of the descending brain-stem pathways Brain 91 1 1968 15 36
49. H. Lee, and G.A. Shamy Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons Stem Cells 25 8 2007 1931 1939 (Pubitemid 47258171)
50. G. Lee, and E.P. Papapetrou Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs Nature 461 7262 2009 402 406
51. R.N. Lemon, and J. Griffiths Comparing the function of the corticospinal system in different species: organizational differences for motor specialization? Muscle Nerve 32 3 2005 261 279 (Pubitemid 41232610)
52. R.N. Lemon, and P.A. Kirkwood Direct and indirect pathways for corticospinal control of upper limb motoneurons in the primate Prog. Brain Res. 143 2004 263 279 (Pubitemid 37443001)
53. X.J. Li, and Z.W. Du Specification of motoneurons from human embryonic stem cells Nat. Biotechnol. 23 2 2005 215 221
54. X.J. Li, and X. Zhang Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells Development 136 23 2009 4055 4063
55. D.D. Licatalosi, A. Mele, J.J. Fak, J. Ule, M. Kayikci, S.W. Chi, T.A. Clark, A.C. Schweitzer, J.E. Blume, X. Wang, J.C. Darnell, and R.B. Darnell HITS-CLIP yields genome-wide insights into brain alternative RNA processing Nature 456 7221 2008 464 469 (Pubitemid 352759008)
56. T. Lin, and R. Ambasudhan A chemical platform for improved induction of human iPSCs Nat. Methods 6 11 2009 805 808
57. M. Lin, E. Pedrosa, A. Shah, A. Hrabovsky, S. Maqbool, D. Zheng, and H.M. Lachman RNA-Seq of human neurons derived from iPS cells reveals candidate long non-coding RNAs involved in neurogenesis and neuropsychiatric disorders PLoS One 6 9 2011 e23356
58. C.L. Liquori, and K. Ricker Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9 Science 293 5531 2001 864 867 (Pubitemid 32743976)
59. R. Lister, and M. Pelizzola Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells Nature 471 7336 2011 68 73
60. F. Liu, and C.X. Gong Tau exon 10 alternative splicing and tauopathies Mol. Neurodegener. 3 2008 8
61. K.E. Lukong, and K.W. Chang RNA-binding proteins in human genetic disease Trends Genet. 24 8 2008 416 425
62. M. Lynch, and J.S. Conery The origins of genome complexity Science 302 5649 2003 1401 1404 (Pubitemid 37452183)
63. N. Maherali, and K. Hochedlinger Tgfbeta signal inhibition cooperates in the induction of iPSCs and replaces Sox2 and cMyc Curr. Biol. 19 20 2009 1718 1723
64. E.V. Makeyev, J. Zhang, M.A. Carrasco, and T. Maniatis The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing Mol. Cell 27 3 2007 435 448 (Pubitemid 47126944)
65. T. Maniatis, and R. Reed An extensive network of coupling among gene expression machines Nature 416 6880 2002 499 506 (Pubitemid 34288845)
66. M.C. Marchetto, and C. Carromeu A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells Cell 143 4 2010 527 539
67. J.W. Marshall, R.M. Cummings, L.J. Bowes, R.M. Ridley, and A.R. Green Functional and histological evidence for the protective effect of NXY-059 in a primate model of stroke when given 4 hours after occlusion Stroke 34 9 2003 2228 2233 (Pubitemid 37099841)
68. N. Miyoshi, H. Ishii, H. Nagano, N. Haraguchi, D.L. Dewi, Y. Kano, S. Nishikawa, M. Tanemura, K. Mimori, F. Tanaka, T. Saito, J. Nishimura, I. Takemasa, T. Mizushima, M. Ikeda, H. Yamamoto, M. Sekimoto, Y. Doki, and M. Mori Reprogramming of mouse and human cells to pluripotency using mature microRNAs Cell Stem Cell 8 6 2011 633 638
69. U.R. Monani, and M. Sendtner The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy Hum. Mol. Genet. 9 3 2000 333 339 (Pubitemid 30098725)
70. G.D. Muir, and I.Q. Whishaw Complete locomotor recovery following corticospinal tract lesions: measurement of ground reaction forces during overground locomotion in rats Behav. Brain Res. 103 1 1999 45 53 (Pubitemid 29447702)
71. M. Nagai, and D.B. Re Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons Nat. Neurosci. 10 5 2007 615 622 (Pubitemid 46652435)
72. M. Nakagawa, M. Koyanagi, K. Tanabe, K. Takahashi, T. Ichisaka, T. Aoi, K. Okita, Y. Mochiduki, N. Takizawa, and S. Yamanaka Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts Nat. Biotechnol. 26 1 2008 101 106
73. M. Nakagawa, and N. Takizawa Promotion of direct reprogramming by transformation-deficient Myc Proc. Natl. Acad. Sci. U. S. A. 107 32 2010 14152 14157
74. S. Nakagawa, T. Naganuma, G. Shioi, and T. Hirose Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice J. Cell Biol. 4 193(1) 2011 31 39
75. P.W. Nathan Effects on movement of surgical incisions into the human spinal cord Brain 117 Pt 2 1994 337 346 (Pubitemid 24155505)
76. J.P. Nemes, and K.A. Benzow The SCA8 transcript is an antisense RNA to a brain-specific transcript encoding a novel actin-binding protein (KLHL1) Hum. Mol. Genet. 9 10 2000 1543 1551 (Pubitemid 30386709)
77. H.N. Nguyen, and B. Byers LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress Cell Stem Cell 8 3 2011 267 280
78. T.W. Nilsen The spliceosome: the most complex macromolecular machine in the cell? Bioessays 25 12 2003 1147 1149 (Pubitemid 37499313)
79. Q. Pan, and O. Shai Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing Nat. Genet. 40 12 2008 1413 1415
80. S. Papadia, and F.X. Soriano Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses Nat. Neurosci. 11 4 2008 476 487 (Pubitemid 351441886)
81. R. Patani, and A. Compston Activin/Nodal inhibition alone accelerates highly efficient neural conversion from human embryonic stem cells and imposes a caudal positional identity PLoS One 4 10 2009 e7327
82. R. Patani, and A.J. Hollins Retinoid-independent motor neurogenesis from human embryonic stem cells reveals a medial columnar ground state Nat. Commun. 2 2011 214
83. A.L. Perrier, and V. Tabar Derivation of midbrain dopamine neurons from human embryonic stem cells Proc. Natl. Acad. Sci. U. S. A. 101 34 2004 12543 12548 (Pubitemid 39122060)
84. A.E. Renton, and E. Majounie A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD Neuron 72 2 2011 257 268
85. E.M. Rouiller, and V. Moret Evidence for direct connections between the hand region of the supplementary motor area and cervical motoneurons in the macaque monkey Eur. J. Neurosci. 8 5 1996 1055 1059 (Pubitemid 26148367)
86. A. Sanchez-Danes, and A. Consiglio Efficient generation of A9 midbrain dopaminergic neurons by lentiviral delivery of LMX1A in human embryonic stem cells and induced pluripotent stem cells Hum. Gene Ther. 2011 Nov 17. [Epub ahead of print]
87. E. Schmidlin, and T. Wannier Progressive plastic changes in the hand representation of the primary motor cortex parallel incomplete recovery from a unilateral section of the corticospinal tract at cervical level in monkeys Brain Res. 1017 1-2 2004 172 183 (Pubitemid 38917157)
88. T.C. Schulz, and S.A. Noggle Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture Stem Cells 22 7 2004 1218 1238 (Pubitemid 39636400)
89. V. Sebastiano, and M.L. Maeder In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases Stem Cells 29 11 2011 1717 1726
90. A. Shuaib, and K.R. Lees NXY-059 for the treatment of acute ischemic stroke N. Engl. J. Med. 357 6 2007 562 571 (Pubitemid 47236281)
91. J.R. Smith, and L. Vallier Inhibition of Activin/Nodal signaling promotes specification of human embryonic stem cells into neuroectoderm Dev. Biol. 313 1 2008 107 117 (Pubitemid 350298306)
92. J. Sreedharan, and I.P. Blair TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis Science 319 5870 2008 1668 1672 (Pubitemid 351432505)
93. P. Stojkovic, and M. Lako Human-serum matrix supports undifferentiated growth of human embryonic stem cells Stem Cells 23 7 2005 895 902 (Pubitemid 41170945)
94. P. Stojkovic, and M. Lako An autogeneic feeder cell system that efficiently supports growth of undifferentiated human embryonic stem cells Stem Cells 23 3 2005 306 314 (Pubitemid 40404449)
95. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 4 2006 663 676 (Pubitemid 44233629)
96. K. Takahashi, and K. Tanabe Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 5 2007 861 872 (Pubitemid 350138099)
97. K. Talbot, and K.E. Davies Spinal muscular atrophy Semin. Neurol. 21 2 2001 189 197 (Pubitemid 32578730)
98. J.A. Thomson, and J. Itskovitz-Eldor Embryonic stem cell lines derived from human blastocysts Science 282 5391 1998 1145 1147 (Pubitemid 28516247)
99. L.T. Timchenko, and N.A. Timchenko Novel proteins with binding specificity for DNA CTG repeats and RNA CUG repeats: implications for myotonic dystrophy Hum. Mol. Genet. 5 1 1996 115 121 (Pubitemid 26018282)
100. J.R. Tollervey, and T. Curk Characterizing the RNA targets and position-dependent splicing regulation by TDP-43 Nat. Neurosci. 14 4 2011 452 458
101. T. Tsukiyama, R. Asano, T. Kawaguchi, N. Kim, M. Yamada, N. Minami, Y. Ohinata, and H. Imai Simple and efficient method for generation of induced pluripotent stem cells using piggyBac transposition of doxycycline-inducible factors and an EOS reporter system Genes Cells 16 7 2011 815 825
102. B.A. Tucker, T.E. Scheetz, R.F. Mullins, A.P. DeLuca, J.M. Hoffmann, R.M. Johnston, S.G. Jacobson, V.C. Sheffield, and E.M. Stone Exome sequencing and analysis of induced pluripotent stem cells identify the cilia-related gene male germ cell-associated kinase (MAK) as a cause of retinitis pigmentosa Proc. Natl. Acad. Sci. U. S. A. 23 108(34) 2011 E569 E576
103. M.H. Tuszynski, and R. Grill Spontaneous and augmented growth of axons in the primate spinal cord: effects of local injury and nerve growth factor-secreting cell grafts J. Comp. Neurol. 449 1 2002 88 101 (Pubitemid 34625696)
104. J. Ule, A. Ule, J. Spencer, A. Williams, J.S. Hu, M. Cline, H. Wang, T. Clark, C. Fraser, M. Ruggiu, B.R. Zeeberg, D. Kane, J.N. Weinstein, J. Blume, and R.B. Darnell Nova regulates brain-specific splicing to shape the synapse Nat. Genet. 37 8 2005 844 852 (Pubitemid 41077110)
105. L. Vallier, and R. Pedersen Differentiation of human embryonic stem cells in adherent and in chemically defined culture conditions Curr. Protoc. Stem Cell Biol. 2008 (Chapter 1: Unit 1D 4 1-1D 4 7)
106. C. Vance, and B. Rogelj Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6 Science 323 5918 2009 1208 1211
107. Y.H. Wang, and J. Griffith Expanded CTG triplet blocks from the myotonic dystrophy gene create the strongest known natural nucleosome positioning elements Genomics 25 2 1995 570 573
108. J. Wang, and E. Pegoraro Myotonic dystrophy: evidence for a possible dominant-negative RNA mutation Hum. Mol. Genet. 4 4 1995 599 606
109. G.S. Wang, and D.L. Kearney Elevation of RNA-binding protein CUGBP1 is an early event in an inducible heart-specific mouse model of myotonic dystrophy J. Clin. Invest. 117 10 2007 2802 2811 (Pubitemid 47529611)
110. E.T. Wang, and R. Sandberg Alternative isoform regulation in human tissue transcriptomes Nature 456 7221 2008 470 476 (Pubitemid 352759009)
111. L. Warren, and P.D. Manos Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA Cell Stem Cell 7 5 2010 618 630
112. H. Wichterle, and S. Przedborski What can pluripotent stem cells teach us about neurodegenerative diseases? Nat. Neurosci. 13 7 2010 800 804
113. C.L. Will, and R. Luhrmann Spliceosomal UsnRNP biogenesis, structure and function Curr. Opin. Cell Biol. 13 3 2001 290 301 (Pubitemid 32429493)
114. B. Wirth, and L. Brichta Spinal muscular atrophy and therapeutic prospects Prog. Mol. Subcell. Biol. 44 2006 109 132
115. B. Wirth, and L. Brichta Spinal muscular atrophy: from gene to therapy Semin. Pediatr. Neurol. 13 2 2006 121 131 (Pubitemid 44486827)
116. J.T. Witten, and J. Ule Understanding splicing regulation through RNA splicing maps Trends Genet. 27 3 2011 89 97
117. C. Xu, and M.S. Inokuma Feeder-free growth of undifferentiated human embryonic stem cells Nat. Biotechnol. 19 10 2001 971 974 (Pubitemid 32947578)
118. S. Yao, and S. Chen Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions Proc. Natl. Acad. Sci. U. S. A. 103 18 2006 6907 6912
119. D.M. Yellon, and D.J. Hausenloy Myocardial reperfusion injury N. Engl. J. Med. 357 11 2007 1121 1135
120. H. Zhou, and S. Wu Generation of induced pluripotent stem cells using recombinant proteins Cell Stem Cell 4 5 2009 381 384
121. S.C. Zhang Neural subtype specification from embryonic stem cells Brain Pathol. 16 2 2006 132 142
122. J. Zou, and M.L. Maeder Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells Cell Stem Cell 5 1 2009 97 110
123. J. Zou, and P. Mali Site-specific gene correction of a point mutation in human iPS cells derived from an adult patient with sickle cell disease Blood 118 17 2011 4599-608
124. J. Zou, and C.L. Sweeney Oxidase-deficient neutrophils from X-linked chronic granulomatous disease iPS cells: functional correction by zinc finger nuclease-mediated safe harbor targeting Blood 117 21 2011 5561 5572