Neurotrophic requirements of human motor neurons defined using amplified and purified stem cell-derived cultures

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Lamas, Nuno Jorge ^a,b,c,d   Kerner, Bethany Johnson ^a,b   Roybon, Laurent ^a,b   Kim, Yoon A ^a   Diaz, Alejandro Garcia ^a   Wichterle, Hynek ^a,b   Henderson, Christopher E ^a,b,e  

^a Project ALS/Jenifer Estess Laboratory for Stem Cell Research   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c UNIVERSITY OF MINHO   (Portugal)

^d UNIVERSITY OF MINHO   (Portugal)

^e LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; CYCLIC AMP; FORSKOLIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN; ISOBUTYLMETHYLXANTHINE; RETINOIC ACID; AMIDE; BRAIN-DERIVED NEUROTROPHIC FACTOR, HUMAN; PROTEIN KINASE INHIBITOR; PYRIDINE DERIVATIVE; RHO KINASE;

ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EC50; EMBRYOID BODY; EMBRYONIC STEM CELL; GENE; HOMEOBOX GENE 9; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MOTONEURON; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEUROTROPISM; PLURIPOTENT STEM CELL; PROMOTER REGION; AGONISTS; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION; GENETICS; METABOLISM;

1-METHYL-3-ISOBUTYLXANTHINE; AMIDES; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CILIARY NEUROTROPHIC FACTOR; COLFORSIN; CYCLIC AMP; EMBRYONIC STEM CELLS; GENE EXPRESSION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MOTOR NEURONS; PROTEIN KINASE INHIBITORS; PYRIDINES; RHO-ASSOCIATED KINASES;

EID: 84908587490     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110324     Document Type: Article

References (59)

1. Han SS, Williams LA, Eggan KC (2011) Constructing and deconstructing stem cell models of neurological disease. Neuron 70: 626-644.
2. Wichterle H, Lieberam I, Porter JA, Jessell TM (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110: 385-397.
3. Li XJ, Du ZW, Zarnowska ED, Pankratz M, Hansen LO, et al. (2005) Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 23: 215-221.
4. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, et al. (2008) Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321: 1218-1221.
5. Ebert AD, Yu J, Rose FF, Jr., Mattis VB, Lorson CL, et al. (2009) Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457: 277-280.
6. Boulting GL, Kiskinis E, Croft GF, Amoroso MW, Oakley DH, et al. (2011) A functionally characterized test set of human induced pluripotent stem cells. Nat Biotechnol 29: 279-286.
7. Hu BY, Weick JP, Yu J, Ma LX, Zhang XQ, et al. (2010) Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc Natl Acad Sci U S A 107: 4335-4340.
8. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, et al. (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27: 275-280.
9. Beck M, Karch C, Wiese S, Sendtner M (2001) Motoneuron cell death and neurotrophic factors: basic models for development of new therapeutic strategies in ALS. Amyotroph Lateral Scler Other Motor Neuron Disord 2 Suppl 1: S55-68.
10. Sendtner M, Pei G, Beck M, Schweizer U, Wiese S (2000) Developmental motoneuron cell death and neurotrophic factors. Cell Tissue Res 301: 71-84.
11. Kanning KC, Kaplan A, Henderson CE (2010) Motor neuron diversity in development and disease. Annu Rev Neurosci 33: 409-440.
12. Raoul C, Buhler E, Sadeghi C, Jacquier A, Aebischer P, et al. (2006) Chronic activation in presymptomatic amyotrophic lateral sclerosis (ALS) mice of a feedback loop involving Fas, Daxx, and FasL. Proc Natl Acad Sci U S A 103:6007-6012.
13. Yan Q, Matheson C, Lopez OT (1995) In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 373: 341-344.
14. Li L, Wu W, Lin LF, Lei M, Oppenheim RW, et al. (1995) Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc Natl Acad Sci U S A 92: 9771-9775.
15. Gould TW, Oppenheim RW (2011) Motor neuron trophic factors: therapeutic use in ALS? Brain Res Rev 67: 1-39.
16. Pennica D, Arce V, Swanson TA, Vejsada R, Pollock RA, et al. (1996) Cardiotrophin-1, a cytokine present in embryonic muscle, supports long-term survival of spinal motoneurons. Neuron 17: 63-74.
17. Sendtner M, Schmalbruch H, Stockli KA, Carroll P, Kreutzberg GW, et al. (1992) Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature 358: 502-504.
18. Oppenheim RW, Prevette D, Yin QW, Collins F, MacDonald J (1991) Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 251: 1616-1618.
19. Koliatsos VE, Clatterbuck RE, Winslow JW, Cayouette MH, Price DL (1993) Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10: 359-367.
20. Oppenheim RW, Yin QW, Prevette D, Yan Q (1992) Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360: 755-757.
21. Singh Roy N, Nakano T, Xuing L, Kang J, Nedergaard M, et al. (2005) Enhancer-specified GFP-based FACS purification of human spinal motor neurons from embryonic stem cells. Exp Neurol 196: 224-234.
22. Di Giorgio FP, Boulting GL, Bobrowicz S, 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.
23. Yang YM, Gupta SK, Kim KJ, Powers BE, Cerqueira A, et al. (2013) A small molecule screen in stem-cell-derived motor neurons identifies a kinase inhibitor as a candidate therapeutic for ALS. Cell Stem Cell 12: 713-726.
24. Kiskinis E, Sandoe J, Williams LA, Boulting GL, Moccia R, et al. (2014) Pathways Disrupted in Human ALS Motor Neurons Identified through Genetic Correction of Mutant SOD1. Cell Stem Cell.
25. Novitch BG, Chen AI, Jessell TM (2001) Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31: 773-789.
26. Zhou Q, Choi G, Anderson DJ (2001) The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31: 791-807.
27. Bayer SA, Altman J (2002) Atlas of human central nervous system development. Boca Raton: CRC Press. v. p.
28. Amoroso MW, Croft GF, Williams DJ, O'Keeffe S, Carrasco MA, et al. (2013) Accelerated high-yield generation of limb-innervating motor neurons from human stem cells. J Neurosci 33: 574-586.
29. Henderson CE, Phillips HS, Pollock RA, Davies AM, Lemeulle C, et al. (1994) GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266: 1062-1064.
30. Mettling C, Camu W, Henderson CE (1993) Embryonic wing and leg motoneurons have intrinsically different survival properties. Development 118:1149-1156.
31. Ullian EM, Harris BT, Wu A, Chan JR, Barres BA (2004) Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture. Mol Cell Neurosci 25: 241-251.
32. Park H, Poo MM (2013) Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 14: 7-23.
33. Gould TW, Enomoto H (2009) Neurotrophic modulation of motor neuron development. Neuroscientist 15: 105-116.
34. Dasen JS, Jessell TM (2009) Hox networks and the origins of motor neuron diversity. Curr Top Dev Biol 88: 169-200.
35. Dasen JS, De Camilli A, Wang B, Tucker PW, Jessell TM (2008) Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 134: 304-316.
36. Henderson CE, Camu W, Mettling C, Gouin A, Poulsen K, et al. (1993) Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363: 266-270.
37. Bordet T, Buisson B, Michaud M, Drouot C, Galea P, et al. (2007) Identification and characterization of cholest-4-en-3-one, oxime (TRO19622), a novel drug candidate for amyotrophic lateral sclerosis. J Pharmacol Exp Ther 322: 709-720.
38. Hanson MG, Jr., Shen S, Wiemelt AP, McMorris FA, Barres BA (1998) Cyclic AMP elevation is sufficient to promote the survival of spinal motor neurons in vitro. J Neurosci 18: 7361-7371.
39. Meyer-FrankeA GAWilkinson KruttgenA HuM MunroE alet 1998 Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons Neuron 21 681-693.
40. Magal E, Burnham P, Varon S (1991) Effects of ciliary neuronotrophic factor on rat spinal cord neurons in vitro: survival and expression of choline acetyltransferase and low-affinity nerve growth factor receptors. Brain Res Dev Brain Res 63: 141-150.
41. Peljto M, Dasen JS, Mazzoni EO, Jessell TM, Wichterle H (2010) Functional diversity of ESC-derived motor neuron subtypes revealed through intraspinal transplantation. Cell Stem Cell 7: 355-366.
42. Street CA, Routhier AA, Spencer C, Perkins AL, Masterjohn K, et al. (2010) Pharmacological inhibition of Rho-kinase (ROCK) signaling enhances cisplatin resistance in neuroblastoma cells. Int J Oncol 37: 1297-1305.
43. Yu Z, Liu M, Fu P, Xie M, Wang W, et al. (2012) ROCK inhibition with Y27632 promotes the proliferation and cell cycle progression of cultured astrocyte from spinal cord. Neurochem Int 61: 1114-1120.
44. Okumura N, Ueno M, Koizumi N, Sakamoto Y, Hirata K, et al. (2009) Enhancement on primate corneal endothelial cell survival in vitro by a ROCK inhibitor. Invest Ophthalmol Vis Sci 50: 3680-3687.
45. Mettling C, Gouin A, Robinson M, el M'Hamdi H, Camu W, et al. (1995) Survival of newly postmitotic motoneurons is transiently independent of exogenous trophic support. J Neurosci 15: 3128-3137.
46. Gauthaman K, Fong CY, Bongso A (2010) Effect of ROCK inhibitor Y-27632 on normal and variant human embryonic stem cells (hESCs) in vitro: its benefits in hESC expansion. Stem Cell Rev 6: 86-95.
47. Routhier A, Astuccio M, Lahey D, Monfredo N, Johnson A, et al. (2010) Pharmacological inhibition of Rho-kinase signaling with Y-27632 blocks melanoma tumor growth. Oncol Rep 23: 861-867.
48. Bueno C, Montes R, Menendez P (2010) The ROCK inhibitor Y-27632 negatively affects the expansion/survival of both fresh and cryopreserved cord blood-derived CD34+ hematopoietic progenitor cells: Y-27632 negatively affects the expansion/survival of CD34+HSPCs. Stem Cell Rev 6: 215-223.
49. Iwamoto H, Nakamuta M, Tada S, Sugimoto R, Enjoji M, et al. (2000) A p160ROCK-specific inhibitor, Y-27632, attenuates rat hepatic stellate cell growth. J Hepatol 32: 762-770.
50. Rees RW, Foxwell NA, Ralph DJ, Kell PD, Moncada S, et al. (2003) Y-27632, a Rho-kinase inhibitor, inhibits proliferation and adrenergic contraction of prostatic smooth muscle cells. J Urol 170: 2517-2522.
51. Julien S, Schnichels S, Teng H, Tassew N, Henke-Fahle S, et al. (2008) Purkinje cell survival in organotypic cultures: implication of Rho and its downstream effector ROCK. J Neurosci Res 86: 531-536.
52. Lingor P, Tonges L, Pieper N, Bermel C, Barski E, et al. (2008) ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain 131: 250-263.
53. Gisselsson L, Toresson H, Ruscher K, Wieloch T (2010) Rho kinase inhibition protects CA1 cells in organotypic hippocampal slices during in vitro ischemia. Brain Res 1316: 92-100.
54. Fournier AE, Takizawa BT, Strittmatter SM (2003) Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 23: 1416-1423.
55. Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, et al. (2002) Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 22: 6570-6577.
56. Lingor P, Teusch N, Schwarz K, Mueller R, Mack H, et al. (2007) Inhibition of Rho kinase (ROCK) increases neurite outgrowth on chondroitin sulphate proteoglycan in vitro and axonal regeneration in the adult optic nerve in vivo. J Neurochem 103: 181-189.
57. Nguyen HN, Byers B, Cord B, Shcheglovitov A, Byrne J, et al. (2011) LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 8: 267-280.
58. Bowerman M, Beauvais A, Anderson CL, Kothary R (2010) Rho-kinase inactivation prolongs survival of an intermediate SMA mouse model. Hum Mol Genet 19: 1468-1478.
59. Kiskinis E, Sandoe J, Williams LA, Boulting GL, Moccia R, et al. (2014) Pathways disrupted in human ALS motor neurons identified through genetic correction of mutant SOD1. Cell Stem Cell 14: 781-795.