Rapid and efficient generation of functional motor neurons from human pluripotent stem cells using gene delivered transcription factor codes

Molecular Therapy

Volumn 19, Issue 10, 2011, Pages 1905-1912

  Hester, Mark E ^a   Murtha, Matthew J ^a,b   Song, Sungwon ^a   Rao, Meghan ^a   Miranda, Carlos J ^a   Meyer, Kathrin ^a   Tian, Jinbin ^b   Boulting, Gabriella ^c,d,e   Schaffer, David V ^f   Zhu, Michael X ^b   Pfaff, Samuel L ^c   Gage, Fred H ^g   Kaspar, Brian K ^a,b  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d Harvard University   (United States)

^e HARVARD UNIVERSITY   (United States)

^f University of California   (United States)

^g SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ALKALINE PHOSPHATASE; LENTIVIRUS VECTOR; NEUROGENIN 2; OCTAMER TRANSCRIPTION FACTOR 4; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ISLET 1; TRANSCRIPTION FACTOR LHX3; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL DIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOTONEURON; NEUROMUSCULAR SYNAPSE; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SPINAL MUSCULAR ATROPHY; STEM CELL GENE THERAPY; VIRAL GENE DELIVERY SYSTEM;

ERINACEIDAE;

EID: 80053575220     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2011.135     Document Type: Article

References (50)

1. Foust, KD, Wang, X, McGovern, VL, Braun, L, Bevan, AK, Haidet, AM et al. (2010). Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol 28: 271-274.
2. Dominguez, E, Marais, T, Chatauret, N, Benkhelifa-Ziyyat, S, Duque, S, Ravassard, P et al. (2011). Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice. Hum Mol Genet 20: 681-693.
3. Passini, MA, Bu, J, Roskelley, EM, Richards, AM, Sardi, SP, O'Riordan, CR et al. (2010). CNS-targeted gene therapy improves survival and motor function in a mouse model of spinal muscular atrophy. J Clin Invest 120: 1253-1264.
4. Valori, CF, Ning, K, Wyles, M, Mead, RJ, Grierson, AJ, Shaw, PJ et al. (2010). Systemic delivery of scAAV9 expressing SMN prolongs survival in a model of spinal muscular atrophy. Sci Transl Med 2: 35ra42.
5. Ebert, AD, Yu, J, Rose, FF Jr, Mattis, VB, Lorson, CL, Thomson, JA et al. (2009). Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457: 277-280.
6. Rossi, SL, Nistor, G, Wyatt, T, Yin, HZ, Poole, AJ, Weiss, JH et al. (2010). Histological and functional benefit following transplantation of motor neuron progenitors to the injured rat spinal cord. PLoS ONE 5: e11852.
7. Corti, S, Nizzardo, M, Nardini, M, Donadoni, C, Salani, S, Ronchi, D et al. (2008). Neural stem cell transplantation can ameliorate the phenotype of a mouse model of spinal muscular atrophy. J Clin Invest 118: 3316-3330.
8. Nagai, M, Re, DB, Nagata, T, Chalazonitis, A, Jessell, TM, Wichterle, H et al. (2007). Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10: 615-622. (Pubitemid 46652435)
9. Di Giorgio, FP, Carrasco, MA, Siao, MC, Maniatis, T and Eggan, K (2007). Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 10: 608-614. (Pubitemid 46652442)
10. Dodge, JC, Haidet, AM, Yang, W, Passini, MA, Hester, M, Clarke, J et al. (2008). Delivery of AAV-IGF-1 to the CNS extends survival in ALS mice through modification of aberrant glial cell activity. Mol Ther 16: 1056-1064. (Pubitemid 351737070)
11. Dodge, JC, Treleaven, CM, Fidler, JA, Hester, M, Haidet, A, Handy, C et al. (2010). AAV4-mediated expression of IGF-1 and VEGF within cellular components of the ventricular system improves survival outcome in familial ALS mice. Mol Ther 18: 2075-2084.
12. Di Giorgio, FP, Boulting, GL, Bobrowicz, S and Eggan, KC (2008). 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: 637-648.
13. Marchetto, MC, Muotri, AR, Mu, Y, Smith, AM, Cezar, GG and Gage, FH (2008). Noncell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 3: 649-657.
14. Wichterle, H, Lieberam, I, Porter, JA and Jessell, TM (2002). Directed differentiation of embryonic stem cells into motor neurons. Cell 110: 385-397.
15. Briscoe, J and Ericson, J (2001). Specification of neuronal fates in the ventral neural tube. Curr Opin Neurobiol 11: 43-49. (Pubitemid 32155948)
16. Singh Roy, N, Nakano, T, Xuing, L, Kang, J, Nedergaard, M and Goldman, SA (2005). Enhancer-specified GFP-based FACS purification of human spinal motor neurons from embryonic stem cells. Exp Neurol 196: 224-234. (Pubitemid 41607810)
17. Lee, H, Shamy, GA, Elkabetz, Y, Schofield, CM, Harrsion, NL, Panagiotakos, G et al. (2007). Directed differentiation and transplantation of human embryonic stem cellderived motoneurons. Stem Cells 25: 1931-1939. (Pubitemid 47258171)
18. Li, XJ, Du, ZW, Zarnowska, ED, Pankratz, M, Hansen, LO, Pearce, RA et al. (2005). Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 23: 215-221. (Pubitemid 40255332)
19. Shin, S, Dalton, S and Stice, SL (2005). Human motor neuron differentiation from human embryonic stem cells. Stem Cells Dev 14: 266-269. (Pubitemid 40885250)
20. Lim, UM, Sidhu, KS and Tuch, BE (2006). Derivation of Motor Neurons from three Clonal Human Embryonic Stem Cell Lines. Curr Neurovasc Res 3: 281-288. (Pubitemid 44706252)
21. Hu, BY and Zhang, SC (2009). Differentiation of spinal motor neurons from pluripotent human stem cells. Nat Protoc 4: 1295-1304.
22. Dhara, SK and Stice, SL (2008). Neural differentiation of human embryonic stem cells. J Cell Biochem 105: 633-640.
23. Wu, H, Xu, J, Pang, ZP, Ge, W, Kim, KJ, Blanchi, B et al. (2007). Integrative genomic and functional analyses reveal neuronal subtype differentiation bias in human embryonic stem cell lines. Proc Natl Acad Sci USA 104: 13821-13826. (Pubitemid 350003404)
24. Miles, GB, Yohn, DC, Wichterle, H, Jessell, TM, Rafuse, VF and Brownstone, RM (2004). Functional properties of motoneurons derived from mouse embryonic stem cells. J Neurosci 24: 7848-7858. (Pubitemid 39215689)
25. Johnson, MA, Weick, JP, Pearce, RA and Zhang, SC (2007). Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture. J Neurosci 27: 3069-3077. (Pubitemid 46474121)
26. Lee, SK and Pfaff, SL (2001). Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat Neurosci 4 Suppl: 1183-1191. (Pubitemid 33733107)
27. Pfaff, SL, Mendelsohn, M, Stewart, CL, Edlund, T and Jessell, TM (1996). Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neurondependent step in interneuron differentiation. Cell 84: 309-320. (Pubitemid 26040847)
28. Thaler, JP, Lee, SK, Jurata, LW, Gill, GN and Pfaff, SL (2002). LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 110: 237-249. (Pubitemid 34876551)
29. Shirasaki, R and Pfaff, SL (2002). Transcriptional codes and the control of neuronal identity. Annu Rev Neurosci 25: 251-281. (Pubitemid 34748018)
30. Dasen, JS, De Camilli, A, Wang, B, Tucker, PW and Jessell, TM (2008). Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 134: 304-316. (Pubitemid 352024390)
31. Dasen, JS, Tice, BC, Brenner-Morton, S and Jessell, TM (2005). A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123: 477-491. (Pubitemid 41546677)
32. Dasen, JS, Liu, JP and Jessell, TM (2003). Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425: 926-933. (Pubitemid 37376919)
33. Rousso, DL, Gaber, ZB, Wellik, D, Morrisey, EE and Novitch, BG (2008). Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 59: 226-240. (Pubitemid 352033689)
34. Aoki, T, Ohnishi, H, Oda, Y, Tadokoro, M, Sasao, M, Kato, H et al. (2010). Generation of induced pluripotent stem cells from human adipose-derived stem cells without c-MYC. Tissue Eng Part A 16: 2197-2206.
35. Hester, ME, Song, S, Miranda, CJ, Eagle, A, Schwartz, PH and Kaspar, BK (2009). Two factor reprogramming of human neural stem cells into pluripotency. PLoS ONE 4: e7044.
36. Yu, J, Vodyanik, MA, Smuga-Otto, K, Antosiewicz-Bourget, J, Frane, JL, Tian, S et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
37. Kim, JB, Greber, B, Araúzo-Bravo, MJ, Meyer, J, Park, KI, Zaehres, H et al. (2009). Direct reprogramming of human neural stem cells by OCT4. Nature 461: 649-643.
38. Nakagawa, M, Koyanagi, M, Tanabe, K, Takahashi, K, Ichisaka, T, Aoi, T et al. (2008). Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26: 101-106.
39. Haase, A, Olmer, R, Schwanke, K, Wunderlich, S, Merkert, S, Hess, C et al. (2009). Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 5: 434-441.
40. Kaji, K, Norrby, K, Paca, A, Mileikovsky, M, Mohseni, P and Woltjen, K (2009). Virusfree induction of pluripotency and subsequent excision of reprogramming factors. Nature 458: 771-775.
41. Kim, JB, Zaehres, H, Araúzo-Bravo, MJ and Schöler, HR (2009). Generation of induced pluripotent stem cells from neural stem cells. Nat Protoc 4: 1464-1470.
42. Takahashi, K, Tanabe, K, Ohnuki, M, Narita, M, Ichisaka, T, Tomoda, K et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872. (Pubitemid 350138099)
43. Bock, C, Kiskinis, E, Verstappen, G, Gu, H, Boulting, G, Smith, ZD et al. (2011). Reference Maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 144: 439-452.
44. Park, IH, Arora, N, Huo, H, Maherali, N, Ahfeldt, T, Shimamura, A et al. (2008). Disease-specific induced pluripotent stem cells. Cell 134: 877-886.
45. Jessell, TM (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1: 20-29.
46. Friling, S, Andersson, E, Thompson, LH, Jönsson, ME, Hebsgaard, JB, Nanou, E et al. (2009). Efficient production of mesencephalic dopamine neurons by Lmx1a expression in embryonic stem cells. Proc Natl Acad Sci USA 106: 7613-7618.
47. Dimos, JT, Rodolfa, KT, Niakan, KK, Weisenthal, LM, Mitsumoto, H, Chung, W et al. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321: 1218-1221.
48. Boulting, GL, Kiskinis, E, Croft, GF, Amoroso, MW, Oakley, DH, Wainger, BJ et al. (2011). A functionally characterized test set of human induced pluripotent stem cells. Nat Biotechnol 29: 279-286.
49. Thomson, JA, Itskovitz-Eldor, J, Shapiro, SS, Waknitz, MA, Swiergiel, JJ, Marshall, VS et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147. (Pubitemid 28516247)
50. Kafri, T, Blömer, U, Peterson, DA, Gage, FH and Verma, IM (1997). Sustained expression of genes delivered directly into liver and muscle by lentiviral vectors. Nat Genet 17: 314-317. (Pubitemid 27475995)