Transcription factor-induced lineage programming of noradrenaline and motor neurons from embryonic stem cells

Stem Cells

Volumn 32, Issue 3, 2014, Pages 609-622

  Mong, Jamie ^a,b,c   Panman, Lia ^a,b,d   Alekseenko, Zhanna ^b   Kee, Nigel ^a,b   Stanton, Lawrence W ^c,e,f   Ericson, Johan ^b   Perlmann, Thomas ^a,b  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c GENOME INSTITUTE OF SINGAPORE   (Singapore)

^d MRC TOXICOLOGY UNIT   (United Kingdom)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

cell programming; drug screening; motor neuron; noradrenaline; noradrenergic; pluripotent; Stem cell

Indexed keywords

CELL PROGRAMMING; DRUG SCREENING; MOTOR NEURON; NORADRENALINE; NORADRENERGIC; PLURIPOTENT; STEM CELL;

ADRENERGIC NEURONS; ANIMALS; CELL LINE; CELL LINEAGE; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENOME; HOMEODOMAIN PROTEINS; HUMANS; MICE; MOTOR NEURONS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84894264796     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1585     Document Type: Article

References (69)

1. Mauritz C, Schwanke K, Reppel M, et al. Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 2008; 118: 507-517.
2. Kim JH, Auerbach JM, Rodriguez-Gomez JA, et al. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 2002; 418: 50-56.
3. Wernig M, Zhao JP, Pruszak J, et al. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci USA 2008; 105: 5856-5861.
4. D'Amour KA, Agulnick AD, Eliazer S, et al. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 2005; 23: 1534-1541.
5. Agarwal S, Holton KL, Lanza R,. Efficient differentiation of functional hepatocytes from human embryonic stem cells. Stem Cells 2008; 26: 1117-1127.
6. Si-Tayeb K, Noto FK, Nagaoka M, et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 2010; 51: 297-305.
7. Maltsev VA, Wobus AM, Rohwedel J, et al. Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents. Circ Res 1994; 75: 233-244.
8. Kobayashi RM, Palkovits M, Kopin IJ, et al. Biochemical mapping of noradrenergic nerves arising from the rat locus coeruleus. Brain Res 1974; 77: 269-279.
9. Swanson LW, Hartman BK,. The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J Comp Neurol 1975; 163: 467-505.
10. Pickel VM, Segal M, Bloom FE,. A radioautographic study of the efferent pathways of the nucleus locus coeruleus. J Comp Neurol 1974; 155: 15-42.
11. Zweig RM, Cardillo JE, Cohen M, et al. The locus ceruleus and dementia in Parkinson's disease. Neurology 1993; 43: 986-991.
12. Cash R, Dennis T, L'Heureux R, et al. Parkinson's disease and dementia: Norepinephrine and dopamine in locus ceruleus. Neurology 1987; 37: 42-46.
13. Chan-Palay V, Asan E,. Alterations in catecholamine neurons of the locus coeruleus in senile dementia of the Alzheimer type and in Parkinson's disease with and without dementia and depression. J Comp Neurol 1989; 287: 373-392.
14. Patt S, Gerhard L,. A Golgi study of human locus coeruleus in normal brains and in Parkinson's disease. Neuropathol Appl Neurobiol 1993; 19: 519-523.
15. Bertrand E, Lechowicz W, Szpak GM, et al. Qualitative and quantitative analysis of locus coeruleus neurons in Parkinson's disease. Folia Neuropathol 1997; 35: 80-86.
16. Zarow C, Lyness SA, Mortimer JA, et al. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 2003; 60: 337-341.
17. Tomlinson BE, Irving D, Blessed G,. Cell loss in the locus coeruleus in senile dementia of Alzheimer type. J Neurol Sci 1981; 49: 419-428.
18. Lyness SA, Zarow C, Chui HC,. Neuron loss in key cholinergic and aminergic nuclei in Alzheimer disease: A meta-analysis. Neurobiol Aging 2003; 24: 1-23.
19. Marien MR, Colpaert FC, Rosenquist AC,. Noradrenergic mechanisms in neurodegenerative diseases: A theory. Brain Res Brain Res Rev 2004; 45: 38-78.
20. Nomura Y, Segawa M,. Anatomy of Rett syndrome. Am J Med Genet Suppl 1986; 1: 289-303.
21. Saito Y, Ito M, Ozawa Y, et al. Reduced expression of neuropeptides can be related to respiratory disturbances in Rett syndrome. Brain Dev 2001; 23 (suppl 1): S122-126.
22. Aroca P, Lorente-Canovas B, Mateos FR, et al. Locus coeruleus neurons originate in alar rhombomere 1 and migrate into the basal plate: Studies in chick and mouse embryos. J Comp Neurol 2006; 496: 802-818.
23. Solloway MJ, Robertson EJ,. Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 1999; 126: 1753-1768.
24. Guo S, Brush J, Teraoka H, et al. Development of noradrenergic neurons in the zebrafish hindbrain requires BMP, FGF8, and the homeodomain protein soulless/Phox2a. Neuron 1999; 24: 555-566.
25. Jaszai J, Reifers F, Picker A, et al. Isthmus-to-midbrain transformation in the absence of midbrain-hindbrain organizer activity. Development 2003; 130: 6611-6623.
26. Holm PC, Rodriguez FJ, Kele J, et al. BMPs, FGF8 and Wnts regulate the differentiation of locus coeruleus noradrenergic neuronal precursors. J Neurochem 2006; 99: 343-352.
27. Lam CS, Sleptsova-Friedrich I, Munro AD, et al. SHH and FGF8 play distinct roles during development of noradrenergic neurons in the locus coeruleus of the zebrafish. Mol Cell Neurosci 2003; 22: 501-515.
28. Tilleman H, Hakim V, Novikov O, et al. Bmp5/7 in concert with the mid-hindbrain organizer control development of noradrenergic locus coeruleus neurons. Mol Cell Neurosci 2010; 45: 1-11.
29. Vogel-Höpker A, Rohrer H,. The specification of noradrenergic locus coeruleus (LC) neurones depends on bone morphogenetic proteins (BMPs). Development 2002; 129: 983-991.
30. Morin X, Cremer H, Hirsch MR, et al. Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a. Neuron 1997; 18: 411-423.
31. Pattyn A,. Specification of the central noradrenergic phenotype by the homeobox gene Phox2b. Mol Cell Neurosci 2000; 15: 235-243.
32. Pattyn A, Morin X, Cremer H, et al. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 1997; 124: 4065-4075.
33. Tiveron MC, Hirsch MR, Brunet JF,. The expression pattern of the transcription factor Phox2 delineates synaptic pathways of the autonomic nervous system. J Neurosci 1996; 16: 7649-7660.
34. Coppola E, Pattyn A, Guthrie SC, et al. Reciprocal gene replacements reveal unique functions for Phox2 genes during neural differentiation. EMBO J 2005; 24: 4392-4403.
35. Pattyn A, Hirsch M, Goridis C, et al. Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 2000; 127: 1349-1358.
36. Marti E, Bumcrot DA, Takada R, et al. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 1995; 375: 322-325.
37. Ericson J, Morton S, Kawakami A, et al. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 1996; 87: 661-673.
38. Panman L, Andersson E, Alekseenko Z, et al. Transcription factor-induced lineage selection of stem-cell-derived neural progenitor cells. Cell Stem Cell 2011; 8: 663-675.
39. Friling S, Andersson E, Thompson LH, et al. Efficient production of mesencephalic dopamine neurons by Lmx1a expression in embryonic stem cells. Proc Natl Acad Sci USA 2009; 106: 7613-7618.
40. Ying Q-L, Stavridis M, Griffiths D, et al. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 2003; 21: 183-186.
41. Schwartz JW, Blakely RD, DeFelice LJ,. Binding and transport in norepinephrine transporters. Real-time, spatially resolved analysis in single cells using a fluorescent substrate. J Biol Chem 2003; 278: 9768-9777.
42. Mason JN, Farmer H, Tomlinson ID, et al. Novel fluorescence-based approaches for the study of biogenic amine transporter localization, activity, and regulation. J Neurosci Methods 2005; 143: 3-25.
43. Jørgensen S, Nielsen EØ, Peters D, et al. Validation of a fluorescence-based high-throughput assay for the measurement of neurotransmitter transporter uptake activity. J Neurosci Methods 2008; 169: 168-176.
44. Oz M, Libby T, Kivell B, et al. Real-time, spatially resolved analysis of serotonin transporter activity and regulation using the fluorescent substrate, ASP++. J Neurochem 2010; 114: 1019-1029.
45. Schwartz JW, Novarino G, Piston DW, et al. Substrate binding stoichiometry and kinetics of the norepinephrine transporter. J Biol Chem 2005; 280: 19177-19184.
46. Haunso A, Buchanan D,. Pharmacological characterization of a fluorescent uptake assay for the noradrenaline transporter. J Biomol Screen 2007; 12: 378-384.
47. Zapata A, Kivell B, Han Y, et al. Regulation of dopamine transporter function and cell surface expression by D3 dopamine receptors. J Biol Chem 2007; 282: 35842-35854.
48. Magrassi L, Purves D, Lichtman JW,. Fluorescent probes that stain living nerve terminals. J Neurosci 1987; 7: 1207-1214.
49. Balice-Gordon RJ, Lichtman JW,. In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse. J Neurosci 1990; 10: 894-908.
50. Melamed N, Rahamimoff R,. Confocal microscopy of the lizard motor nerve terminals. J Basic Clin Physiol Pharmacol 1991; 2: 63-85.
51. Chen LL, Folsom DB, Ko CP,. The remodeling of synaptic extracellular matrix and its dynamic relationship with nerve terminals at living frog neuromuscular junctions. J Neurosci 1991; 11: 2920-2930.
52. Marques MJ, Santo Neto H,. Imaging neuromuscular junctions by confocal fluorescence microscopy: Individual endplates seen in whole muscles with vital intracellular staining of the nerve terminals. J Anat 1998; 192 (Pt 3): 425-430.
53. Kurdyak P, Atwood HL, Stewart BA, et al. Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J Comp Neurol 1994; 350: 463-472.
54. Vaillant GE,. Clinical significance of anticholinergic effects of imipramine-like drugs. Am J Psychiatry 1969; 125: 1600-1602.
55. Szabadi E, Gaszner P, Bradshaw CM,. The peripheral anticholinergic activity of tricyclic antidepressants: Comparison of amitriptyline and desipramine in human volunteers. Br J Psychiatry 1980; 137: 433-439.
56. Weinstock M, Cohen D,. Tricyclic antidepressant drugs as antagonists of muscarinic receptors in sympathetic ganglia. Eur J Pharmacol 1976; 40: 321-328.
57. Nat R, Nilbratt M, Narkilahti S, et al. Neurogenic neuroepithelial and radial glial cells generated from six human embryonic stem cell lines in serum-free suspension and adherent cultures. Glia 2007; 55: 385-399.
58. Chambers SM, Fasano CA, Papapetrou EP, et al. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 2009; 27: 275-280.
59. Itsykson P, Ilouz N, Turetsky T, et al. Derivation of neural precursors from human embryonic stem cells in the presence of noggin. Mol Cell Neurosci 2005; 30: 24-36.
60. Gerrard L, Rodgers L, Cui W,. Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells 2005; 23: 1234-1241.
61. Taneja P, Ogier M, Brooks-Harris G, et al. Pathophysiology of locus ceruleus neurons in a mouse model of Rett syndrome. J Neurosci 2009; 29: 12187-12195.
62. Zhang X, Cui N, Wu Z, et al. Intrinsic membrane properties of locus coeruleus neurons in Mecp2-null mice. Am J Physiol Cell Physiol 2010; 298: C635-646.
63. Hotta A, Cheung AY, Farra N, et al. Isolation of human iPS cells using EOS lentiviral vectors to select for pluripotency. Nat Methods 2009; 6: 370-376.
64. Amenduni M, De Filippis R, Cheung AY, et al. iPS cells to model CDKL5-related disorders. Eur J Hum Genet 2011; 19: 1246-1255.
65. Cheung AY, Horvath LM, Grafodatskaya D, et al. Isolation of MECP2-null Rett Syndrome patient hiPS cells and isogenic controls through X-chromosome inactivation. Hum Mol Genet 2011; 20: 2103-2115.
66. Kim KY, Hysolli E, Park IH,. Neuronal maturation defect in induced pluripotent stem cells from patients with Rett syndrome. Proc Natl Acad Sci USA 2011; 108: 14169-14174.
67. Ananiev G, Williams EC, Li H, et al. Isogenic pairs of wild type and mutant induced pluripotent stem cell (iPSC) lines from Rett syndrome patients as in vitro disease model. PLoS One 2011; 6: e25255.
68. Andersson E, Tryggvason U, Deng Q, et al. Identification of intrinsic determinants of midbrain dopamine neurons. Cell 2006; 124: 393-405.
69. Wichterle H, Lieberam I, Porter JA, et al. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002; 110: 385-397.