Molecular and functional analyses of motor neurons generated from human cord-blood-derived induced pluripotent stem cells

Stem Cells and Development

Volumn 23, Issue 24, 2014, Pages 3011-3020

  Naujock, Maximilian ^a,b,c   Stanslowsky, Nancy ^a,b   Reinhardt, Peter ^d   Sterneckert, Jared ^d   Haase, Alexandra ^a,e   Martin, Ulrich ^a,e   Kim, Kwang Soo ^c   Dengler, Reinhard ^a,b   Wegner, Florian ^a,b   Petri, Susanne ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^e Excellence Cluster REBIRTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND GATED ION CHANNEL; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX1; VIMENTIN; VOLTAGE GATED CHLORIDE CHANNEL; ION CHANNEL;

ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL MEMBRANE DEPOLARIZATION; CORD BLOOD DERIVED INDUCED PLURIPOTENT STEM CELL; CORD BLOOD STEM CELL TRANSPLANTATION; EPIGENETICS; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MOTONEURON; PATCH CLAMP TECHNIQUE; PLURIPOTENT STEM CELL; UPREGULATION; WHOLE CELL PATCH CLAMP; WNT SIGNALING PATHWAY; ACTION POTENTIAL; CELL CULTURE; CYTOLOGY; FETUS BLOOD; GENETICS; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PHYSIOLOGY; SYNAPTIC POTENTIAL;

ACTION POTENTIALS; CELLS, CULTURED; FETAL BLOOD; HUMANS; INDUCED PLURIPOTENT STEM CELLS; ION CHANNELS; MOTOR NEURONS; NEURAL STEM CELLS; NEUROGENESIS; SYNAPTIC POTENTIALS;

EID: 84916881704     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0180     Document Type: Article

References (43)

1. Takahashi K and S Yamanaka. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676
2. Takahashi K, K Tanabe, M Ohnuki, M Narita, T Ichisaka, K Tomoda and S Yamanaka. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872
3. Lee H, GA Shamy, Y Elkabetz, CM Schofield, NL Harrsion, G Panagiotakos, ND Socci, V Tabar and L Studer. (2007). Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons. Stem Cells 25:1931-1939
4. Amoroso MW, GF Croft, DJ Williams, S OKeeffe, MA Carrasco, AR Davis, L Roybon, DH Oakley, T Maniatis, CE Henderson and H Wichterle. (2013). Accelerated highyield generation of limb-innervating motor neurons from human stem cells. J Neurosci 33:574-586
5. Egawa N, S Kitaoka, K Tsukita, M Naitoh, K Takahashi, T Yamamoto, F Adachi, T Kondo, K Okita, et al. (2012). Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci Transl Med 4:145ra104
6. Bilican B, A Serio, SJ Barmada, AL Nishimura, GJ Sullivan, M Carrasco, HP Phatnani, CA Puddifoot, D Story, et al. (2012). Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc Natl Acad Sci U S A 109:5803-5808
7. Sareen D, JG ORourke, P Meera, AK Muhammad, S Grant, M Simpkinson, S Bell, S Carmona, L Ornelas, et al. (2013). Targeting foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci Transl Med 5:208ra149
8. Ebert AD, J Yu, FF Rose Jr., VB Mattis, CL Lorson, JA Thomson and CN Svendsen. (2009). Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457:277-280
9. Chang T, W Zheng, W Tsark, S Bates, H Huang, RJ Lin and JK Yee. (2009). Brief report: phenotypic rescue of induced pluripotent stem cell-derived motoneurons of a spinal muscular atrophy patient. Stem Cells 29:2090-2093
10. Dimos JT, KT Rodolfa, KK Niakan, LM Weisenthal, H Mitsumoto, W Chung, GF Croft, G Saphier, R Leinbel, et al. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321:1218-1221
11. Karumbayaram S, BG Novitch, M Patterson, JA Umbach, L Richter, A Lindgren, AE Conway, AT Clark, SA Goldman, et al. (2009). Directed differentiation of human-induced pluripotent stem cells generates active motor neurons. Stem Cells 27:806-8011
12. Haase A, R Olmer, K Schwanke, S Wunderlich, S Merkert, C Hess, R Zweigerdt, I Gruh, J Meyer, et al. (2009). Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 5:434-441
13. Park TS, I Bhutto, L Zimmerlin, JS Huo, P Nagaria, D Miller, AJ Rufaihah, C Talbot, J Aguilar, et al. (2014). Vascular progenitors from cord blood-derived induced pluripotent stem cells possess augmented capacity for regenerating ischemic retinal vasculature. Circulation 129: 359-372
14. Reinhardt P, M Glatza, K Hemmer, Y Tsytsyura, CS Thiel, S Höing, S Moritz, JA Parga, L Wagner, et al. (2013). Derivation and expansion using only small molecules of numan neural progenitors for neurodegenrative disease modelling. PLoS One 8: e59252
15. Johnson MA, JP Weick, RA Pearce and SC Zhang. (2007). Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture. J Neurosci 27:3069-3077
16. Wada T, M Honda, I Minami, N Tooi, Y Amagai, N Nakatsuji and K Aiba. (2009). Highly efficient differentiation and enrichment of spinal motor neurons derived from human and monkey embryonic stem cells. PLoS One 4: e6722
17. Hu BY, JP Weick, J Yu, LX Ma, XQ Zhang, JA Thomson and SC Zhang. (2010). Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. PNAS 107:4335-4340
18. Stanslowsky N, A Haase, U Martin, M Naujock, A Leffler, R Dengler and F Wegner. (2014). Functional differentiation of midbrain neurons from human cord blood-derived induced pluripotent stem cells. Stem Cell Res Ther 5:35
19. Sonntag KC, J Pruszak, T Yoshizaki, J van Arensbergen, R Sanchez-Pernaute and O Isacson. (2007). Enhanced yield of neuroepithelial precursors and midbrain-like dopaminergic neurons from human embryonic stem cells using the bone morphogenic protein antagonist noggin. Stem Cells 25:411-418
20. Chambers SM, CA Fasano, EP PapapetrouP, M Tomishima, M Sadelain and L Studer. (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27:275-280
21. Kim DS, JS Lee, JW Leem, YJ Huh, JY Kim, HS Kim, ICH Park, GQ Daley, DY Hwang and DW Kim. (2010). Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev 6:270-281
22. Wichterle H, I Lieberam, JA Porter and TM Jessell. (2002). Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385-397
23. Zwart R and HP Vijverberg. (1997). Potentiation and inhibition of neuronal nicotinic receptors by atropine: competitive and noncompetitive effects. Mol Pharmacol 52: 886-895
24. Shen WX and JP Horn. (1997). Mecamylamine selectively blocks nicotinic receptors on vasomotor sympathetic C neurons. Brain Res 788:118-124
25. Nakamizo T, J Kawamata, H Yamashita, R Kanki, H Sawada, A Akaike and S Shimohama. (2005). Stimulation of nicotinic acetylcholine receptors protects motor neurons. Biochem Biophys Res Commun 330:1285-1289
26. Hu BY and SC Zhang. (2009). Differentiation of spinal motor neurons from pluripotent human stem cells. Nat Protoc 4:1295-1304
27. Stockmann M, L Linta, KJ Föhr, A Boeckers, AC Ludolph, GF Kuh, PT Udvardi, C Proepper, A Storch, et al. (2013). Developmental and functional nature of human iPSC derived motoneurons. Stem Cell Rev and Rep 9:475-492
28. Erdö F, C Bührle, J Blunk, M Hoehn, Y Xia, B Fleischmann, M Föcking, E Küstermann, E Kolossov, et al. (2003). Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J Cereb Blood Flow Metab 23:780-785
29. Roy NS, C Clere, SK Singh, L Yang, MF Beal and SA Goldman. (2006). Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat Med 12:1259-1268
30. Hedlund E, J Pruszak, A Ferree, A Vinuela, S Hong, O Isacson and KS Kim. (2007). Selection of embryonic stem cell-derived enhanced green fluorescent protein-positive dopamine neurons using the tyrosine hydroxylase promoter is confounded by reporter gene expression in immature cell populations. Stem Cells 25:1126-1135
31. Pruszak J, KC Sonntag, MH Aung, R Sanchez-Pernaute and O Isacson. (2007). Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 25:2257-2268
32. Kim D, CH Kim, JIMoon, YG Chung, MY Chang, BS Han, S Ko, E Yang, YK Cha, R Lanza and KS Kim. (2009). Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4:472-476
33. Anokye-Danso F, CM Trivedi, D Juhr, M Gupta, Z Ciu, Y Tian, Y Zhang, W Yang, PJ Gruber, JA Epstein and EE Morrisey. (2011). Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8:376-388
34. Lu J, H Liu, C Tzu-Ling Huang, H Cheng, Z Du, Y, Liu, MA Sherafat and SC Zhang (2013). Generation of integration-free and region-specific neural progenitors from primate fibroblasts. Cell Rep 3, 1-12
35. Son EY, JK Ichida, BJ Wainger, JS Toma, VF Rafuse, CJ Woolf and K Eggan. (2011). Conversion of Mouse and Human Fibroblasts into Functional Spinal Motor Neurons. Cell Stem Cell 9:205-218
36. Wegner F, W Deuther-Conrad, M Scheunemann, P Brust, S Fischer, A Hiller, M Diekers, K Strecker, K Wohlfahrt, et al. (2008). GABA A receptor pharmacology of fluorinated derivates of the novel sedative-hypnotic pyrazolopyrimidine indiplon. Eur J Pharmacol 580:1-11
37. Wegner F, R Kraft, K Busse, W Härtig, G Schaarschmidt, SC Schwarz, J Schwarz and W Hevers. (2008). Functional and molecular analysis of GABAA receptors in human midbrain-derived neural progenitor cells. J Neurochem 107: 1056-1069
38. Wegner F, R Kraft, K Busse, W Härtig, J Ahrens, A Leffler, R Dengler and J Schwarz. (2012). Differentiated human midbrain-derived neural progenitor cells express excitatory strychnine-sensitive glycine receptors containing a2b subunits. PLoS One 7:e36946
39. Mauksch C, E Firmin, C Butler-Munro, JM Montgomery, M Dottori and B Connor. (2012). Non-viral generation of neural precursor-like cells from adult human fibroblasts. JSRM 3:162-170
40. Zeng H, M Guo, K Martins-Taylor, X Wang, Z Zhang, JW Park, S Zhan, MS Kronenberg, A Lichtler, et al. (2010). Specification of region-specific neurons including forebrain glutamatergic neurons from human induced pluripotent stem cells. PLoS One 5:e11853
41. Gao BX and L Ziskind-Conhaim. (1998). Development of ionic currents underlying changes in action potential waveforms in rat spinal motoneurons. J Neurophysiol 80: 3047-3061
42. Ullian EM, BT Harris, A Wu, JR Chan and BA Barres. (2004). Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture. Mol Cell Neurosci 25;2:241-251
43. Bai D and DB Sattelle. (1994). Muscarinic acetylcholine receptors on an identified motor neurone in the cockroach, Periplaneta americana. Neurosci Lett 175:161-165.