Physiological characterisation of human iPS-derived dopaminergic neurons

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Hartfield, Elizabeth M ^a,b   Yamasaki Mann, Michiko ^a,b   Ribeiro Fernandes, Hugo J ^a,b   Vowles, Jane ^a,c   James, William S ^a,c   Cowley, Sally A ^a,c   Wade Martins, Richard ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; INOSITOL TRISPHOSPHATE 3 KINASE; TYROSINE 3 MONOOXYGENASE; 1 METHYL 4 PHENYLPYRIDINIUM; CALCIUM; KCNJ6 PROTEIN, HUMAN;

ARTICLE; BRAIN REGION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; DENDRITE; DOPAMINE METABOLISM; DOPAMINE RELEASE; DOPAMINE REUPTAKE; DOPAMINE UPTAKE; DOPAMINERGIC NERVE CELL; ENDOPLASMIC RETICULUM; EXON; FOXA2 GENE; GENE; GENE EXPRESSION; GIRK2 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MESENCEPHALON; MITOCHONDRIAL MEMBRANE POTENTIAL; NUCLEOTIDE SEQUENCE; PARKINSON DISEASE; PLURIPOTENT STEM CELL; SUBSTANTIA NIGRA PARS COMPACTA; CELL CULTURE; CYTOLOGY; EMBRYOID BODY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; METABOLISM; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

1-METHYL-4-PHENYLPYRIDINIUM; BLOTTING, WESTERN; CALCIUM; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOPAMINERGIC NEURONS; EMBRYOID BODIES; ENDOPLASMIC RETICULUM; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; HUMANS; IMMUNOHISTOCHEMISTRY; INDUCED PLURIPOTENT STEM CELLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MESENCEPHALON; PARKINSON DISEASE; PATCH-CLAMP TECHNIQUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TYROSINE 3-MONOOXYGENASE;

EID: 84896800539     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087388     Document Type: Article

References (65)

1. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, et al. (2007) 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 447: 1081-1086. (Pubitemid 47014425)
2. Surmeier DJ (2007) Calcium, ageing, and neuronal vulnerability in Parkinson's disease. Lancet neurol 6: 933-938.
3. Guzman JN, Sanchez-Padilla J, Chan CS, Surmeier DJ (2009) Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci 29: 11011-11019.
4. Nedergaard S, Flatman JA, Engberg I (1993) Nifedipine- and omega-conotoxin-sensitive Ca2+ conductances in guinea-pig substantia nigra pars compacta neurones. J Physiol 466: 727-747. (Pubitemid 23225251)
5. Bolam JP, Pissadaki EK (2012) Living on the edge with too many mouths to feed: Why dopamine neurons die. Mov Disord 27: 1478-1483.
6. Matsuda W, Furuta T, Nakamura KC, Hioki H, Fujiyama F, et al. (2009) Single Nigrostriatal Dopaminergic Neurons Form Widely Spread and Highly Dense Axonal Arborizations in the Neostriatum. J Neurosci 29: 444-453.
7. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-372.
8. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
9. Cooper O, Seo H, Andrabi S, Guardia-Laguarta C, Graziotto J, et al. (2012) Pharmacological rescue of mitochondrial deficits in iPSC-derived neural cells from patients with familial Parkinson's disease. Sci Transl Med 4 (414).
10. Jiang H, Ren Y, Yuen EY, Zhong P, Ghaedi M, et al. (2012) Parkin controls dopamine utilization in human midbrain dopaminergic neurons derived from induced pluripotent stem cells. Nat Commun 3: 668-686.
11. 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.
12. Sanchez-Danes A, Richaud-Patin Y, Carballo-Carbajal I, Jimenez-Delgado S, Caig C, et al. (2012) Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease. EMBO Mol Med 4: 380-395.
13. Seibler P, Graziotto J, Jeong H, Simunovic F, Klein C, et al. (2011) Mitochondrial Parkin recruitment is impaired in neurons derived from mutant PINK1 induced pluripotent stem cells. J Neurosci 31: 5970-5976.
14. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors 131: 861-872.
15. Chia R, Achilli F, Festing MF, Fisher EM (2005)The origins and uses of mouse outbred stocks. Nat genet 37: 1181-1186. (Pubitemid 41568697)
16. Gardner RL (1982) Investigation of cell lineage and differentiation in the extraembryonic endoderm of the mouse embryo. J Embryol Exp Morphol 68: 175-198.
17. Moralli D, Yusuf M, Mandegar M, Khoja S, Monaco Z, et al. (2011) An improved technique for chromosomal analysis of human ES and iPS cells. Stem cell rev 7: 471-477.
18. Muller FJ, Schuldt BM, Williams R, Mason D, Altun G, et al. (2011) A bioinformatic assay for pluripotency in human cells. Nat Methods 8: 315-317.
19. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, et al. (2009) Human Induced Pluripotent Stem Cells Free of Vector and Transgene Sequences. Science 324: 797-801.
20. 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 Biotech 27: 275-280.
21. Cooper O, Hargus G, Deleidi M, Blak A, Osborn T, et al. (2010) Differentiation of human ES and Parkinson's disease iPS cells into ventral midbrain dopaminergic neurons requires a high activity form of SHH, FGF8a and specific regionalization by retinoic acid. Mol Cell Neurosci 45: 258-266.
22. Schneider BL, Seehus CR, Capowski EE, Aebischer P, Zhang SC, et al. (2007) Over-expression of alpha-synuclein in human neural progenitors leads to specific changes in fate and differentiation. Hum Mol Genet 16: 651-666. (Pubitemid 46591118)
23. Reyes S, Fu Y, Double K, Thompson L, Kirik D, et al. (2012) GIRK2 expression in dopamine neurons of the substantia nigra and ventral tegmental area. J Comp Neurol 520: 2591-2607.
24. Hernandez F, Perez M, de Barreda EG, Goni-Oliver P, Avila J (2008) Tau as a molecular marker of development, aging and neurodegenerative disorders. Curr Aging Sci 1: 56-61.
25. Mattson MP (2007) Calcium and neurodegeneration. Aging Cell 6: 337-350.
26. Surmeier DJ, Schumacker PT (2013) Calcium, bioenergetics, and neuronal vulnerability in Parkinson's disease. J Biol Chem 288: 10736-10741.
27. Surmeier DJ, Guzman JN, Sanchez-Padilla J, Goldberg JA (2011) The origins of oxidant stress in Parkinson's disease and therapeutic strategies. Antioxid Redox Signal 14: 1289-2301.
28. Morikawa H, Imani F, Khodakhah K, Williams JT (2000) Inositol 1,4,5-triphosphate-evoked responses in midbrain dopamine neurons. J Neurosci 20: 303-314.
29. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, et al. (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459: 596-600.
30. Patel S, Ramakrishnan L, Rahman T, Hamdoun A, Marchant JS, et al. (2011) The endo-lysosomal system as an NAADP-sensitive acidic Ca(2+) store: role for the two-pore channels. Cell Calcium 50: 157-167.
31. Exner N, Lutz AK, Haass C, Winklhofer KF (2012) Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J 31: 3038-3062.
32. Kitayama S, Shimada S, Xu H, Markham L, Donovan DM, et al. (1992) Dopamine transporter site-directed mutations differentially alter substrate transport and cocaine binding. Proc Natl Acad Sci U S A 89: 7782-7785.
33. Wu S, Zhou F, Zhang Z, Xing D (2011) Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins. FEBS J 278: 941-954.
34. Hussein S, Batada N, Vuoristo S, Ching R, Autio R, et al. (2011) Copy number variation and selection during reprogramming to pluripotency. Nature 471: 58-62.
35. Müller F-J, Goldmann J, Löser P, Loring JF (2010) A Call to Standardize Teratoma Assays Used to Define Human Pluripotent Cell Lines. Cell Stem Cell 6: 412-414.
36. Chan EM, Ratanasirintrawoot S, Park I-H, Manos PD, Loh Y-H, et al. (2009) Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells. Nat Biotech 27: 1033-1037.
37. Koyanagi M, Takahashi J, Arakawa Y, Doi D, Fukuda H, et al. (2008) Inhibition of the Rho/ROCK pathway reduces apoptosis during transplantation of embryonic stem cell-derived neural precursors. J Neurosci Res 86: 270-280. (Pubitemid 351196733)
38. Zhang L, Valdez JM, Zhang B, Wei L, Chang J, et al. (2011) ROCK Inhibitor Y-27632 Suppresses Dissociation-Induced Apoptosis of Murine Prostate Stem/Progenitor Cells and Increases Their Cloning Efficiency. PLoS ONE 6: e18271.
39. Kriks S, Shim JW, Piao J, Ganat YM, Wakeman DR, et al. (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480: 547-551.
40. Iovino M, Patani R, Watts C, Chandran S, Spillantini MG (2010) Human Stem Cell-Derived Neurons: A System to Study Human Tau Function and Dysfunction. PLoS One 5: e13947.
41. Patani R, Lewis PA, Trabzuni D, Puddifoot CA, Wyllie DJ, et al. (2012) Investigating the utility of human embryonic stem cell-derived neurons to model ageing and neurodegenerative disease using whole-genome gene expression and splicing analysis. J Neurochem 122: 738-751.
42. Chung CY, Seo H, Sonntag KC, Brooks A, Lin L, et al. (2005) Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection. Hum Mol Genet 14: 1709-1725. (Pubitemid 41418045)
43. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39: 889-909. (Pubitemid 37130207)
44. Sundberg M, Bogetofte H, Lawson T, Jansson J, Smith G, et al. (2013) Improved Cell Therapy Protocols for Parkinson's Disease Based on Differentiation Efficiency and Safety of hESC-, hiPSC-, and Non-Human Primate iPSC-Derived Dopaminergic Neurons. Stem cells 31: 1548-1562.
45. Badger JL, Cordero-Llana O, Hartfield EM, Wade-Martins R (2014) Parkinson's disease in a dish - Using stem cells as a molecular tool. Neuropharmacology 76: 88-96.
46. Cho MS, Lee YE, Kim JY, Chung S, Cho YH, et al. (2008) Highly efficient and large-scale generation of functional dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A 105: 3392-3397. (Pubitemid 351723563)
47. Nguyen Ha N, 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.
48. Perrier AL, Tabar V, Barberi T, Rubio ME, Bruses J, et al. (2004) Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A 101: 12543-12548. (Pubitemid 39122060)
49. Rhee YH, Ko JY, Chang MY, Yi SH, Kim D, et al. (2011) Protein-based human iPS cells efficiently generate functional dopamine neurons and can treat a rat model of Parkinson disease. J Clin Invest 121: 2326-2335.
50. Tian LP, Zhang S, Zhang YJ, Ding JQ, Chen SD (2012) Lmx1b can promote the differentiation of embryonic stem cells to dopaminergic neurons associated with Parkinson's disease. Biotechnol Lett 34: 1167-1174.
51. Byers B, Cord B, Nguyen HN, Schule B, Fenno L, et al. (2011) SNCA triplication Parkinson's patient's iPSC-derived DA neurons accumulate alpha-synuclein and are susceptible to oxidative stress. PLoS One 6: e26159.
52. Cai J, Yang M, Poremsky E, Kidd S, Schneider JS, et al. (2010) Dopaminergic neurons derived from human induced pluripotent stem cells survive and integrate into 6-OHDA-lesioned rats. Stem Cells Dev 19: 1017-1023.
53. Strömberg I, van Horne C, Bygdeman M, Weiner N, Gerhardt GA (1991) Function of intraventricular human mesencephalic xenografts in immunosuppressed rats: An electrophysiological and neurochemical analysis. Exp Neurol 112: 140-152.
54. Hahn J, Kullmann PH, Horn JP, Levitan ES (2006) D2 autoreceptors chronically enhance dopamine neuron pacemaker activity. J Neurosci 26: 5240-5247. (Pubitemid 44315306)
55. Tepper JM, Trent F, Nakamura S (1990) Postnatal development of the electrical activity of rat nigrostriatal dopaminergic neurons. Brain Res Dev Brain Res 54: 21-33. (Pubitemid 20177647)
56. Amini B, Clark JW Jr, Canavier CC (1999) Calcium dynamics underlying pacemaker-like and burst firing oscillations in midbrain dopaminergic neurons: a computational study. J Neurophysiol 82: 2249-2261.
57. Heyer EJ (1984) Electrophysiological study of mammalian neurons from ventral mesencephalon grown in primary dissociated cell culture. Brain Res 310: 142-148.
58. Kang Y, Kitai ST (1993) Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra. Neurosci Res 18: 195-207. (Pubitemid 24024861)
59. Watmuff B, Pouton CW, Haynes JM (2012) In vitro maturation of dopaminergic neurons derived from mouse embryonic stem cells: implications for transplantation. PLoS One 7: e31999.
60. Surmeier DJ, Guzman JN, Sanchez-Padilla J (2010) Calcium, cellular aging, and selective neuronal vulnerability in Parkinson's disease. Cell Calcium 47: 175-182.
61. Wilson CJ, Callaway JC (2000) Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83: 3084-3100. (Pubitemid 30321496)
62. Mosharov EV, Larsen KE, Kanter E, Phillips KA, Wilson K, et al. (2009) Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons. Neuron 62: 218-229.
63. Porras G, Li Q, Bezard E (2012) Modeling Parkinson's disease in primates: The MPTP model. Cold Spring Harb perspect med 2: a009308.
64. Kitayama S, Mitsuhata C, Davis S, Wang JB, Sato T, et al. (1998) MPP+ toxicity and plasma membrane dopamine transporter: study using cell lines expressing the wild-type and mutant rat dopamine transporters. Biochim biophys acta 1404: 305-313. (Pubitemid 28470532)
65. Cooper O, Seo H, Andrabi S, Guardia-Laguarta C, Graziotto J, et al (2012) Pharmacological Rescue of Mitochondrial Deficits in iPSC-Derived Neural Cells from Patients with Familial Parkinson's Disease. Sci Transl Med 4: 141-166.