Characterization of the NT2-derived neuronal and astrocytic cell lines as alternative in vitro models for primary human neurons and astrocytes

Journal of Neuroscience Research

Volumn 92, Issue 9, 2014, Pages 1187-1198

  Haile, Yohannes ^a   Fu, Wen ^a   Shi, Beipei ^b   Westaway, David ^b   Baker, Glen ^a   Jhamandas, Jack ^a   Giuliani, Fabrizio ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Calcium imaging; Human fetal neurons; Neuronal cell model; Neuronal differentiation; NT2

Indexed keywords

AMINO ACID; CALCIUM; NEUROTRANSMITTER; NEUROTRANSMITTER RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; MAP2 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; TUBB3 PROTEIN, HUMAN; TUBULIN;

ADULT; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL LINE; CELL STRUCTURE; CELL TYPE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FETUS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN FETAL NEURON; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; NERVE CELL; NT2 DERIVED ASTROCYTE; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STIMULATION; BRAIN; CELL CULTURE; CELL SIZE; CYTOLOGY; METABOLISM; PATHOLOGY; TERATOMA; TUMOR CELL LINE;

AMINO ACIDS; ASTROCYTES; BRAIN; CALCIUM; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SIZE; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FETUS; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; RECEPTORS, NEUROTRANSMITTER; TERATOMA; TUBULIN;

EID: 84904259962     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23399     Document Type: Article

References (61)

1. Anderl JL, Redpath S, Ball AJ. 2009. A neuronal and astrocyte co-culture assay for high content analysis of neurotoxicity. J Vis Exp 5:1-6.
2. Andrews PW. 1984. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol 103:285-293.
3. Andrews PW, Damjanov I, Simon D, Banting GS, Carlin C, Dracopoli NC, Fogh J. 1984. Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lab Invest 50:147-162.
4. Beczkowska IW, Gracy KN, Pickel VM, Inturrisi CE. 1997. Inducible expression of N-methyl-D-aspartate receptor, and delta and mu opioid receptor messenger RNAs and protein in the NT2-N human cell line. Neuroscience 79:855-862.
5. Belkind-Gerson J, Carreon-Rodriguez A, Benedict LA, Steiger C, Pieretti A, Nagy N, Dietrich J, Goldstein AM. 2012. Nestin-expressing cells in the gut give rise to enteric neurons and glial cells. Neurogastroenterol Motil 25:61-69.
6. Bramanti V, Bronzi D, Tomassoni D, Costa A, Raciti G, Avitabile M, Amenta F, Avola R. 2008a. Growth factors and steroid mediated regulation of cytoskeletal protein expression in serum-deprived primary astrocyte cultures. Neurochem Res 33:2593-2600.
7. Bramanti V, Bronzi D, Tomassoni D, Li Volti G, Cannavo G, Raciti G, Napoli M, Vanella A, Campisi A, Ientile R, Avola R. 2008b. Effect of choline-containing phospholipids on transglutaminase activity in primary astroglial cell cultures. Clin Exp Hypertens 30:798-807.
8. Bramanti V, Campisi A, Tomassoni D, Li Volti G, Caccamo D, Cannavo G, Curro M, Raciti G, Napoli M, Ientile R, Vanella A, Amenta F, Avola R. 2008c. Effect of acetylcholine precursors on proliferation and differentiation of astroglial cells in primary cultures. Neurochem Res 33:2601-2608.
9. Butt AM. 2011. ATP: a ubiquitous gliotransmitter integrating neuron-glial networks. Semin Cell Dev Biol 22:205-213.
10. Chklovskii DB. 2004. Synaptic connectivity and neuronal morphology: two sides of the same coin. Neuron 43:609-617.
11. Coughlan CM, Mcmanus CM, Sharron M, Gao Z, Murphy D, Jaffer S, Choe W, Chen W, Hesselgesser J, Gaylord H, Kalyuzhny A, Lee VM, Wolf B, Doms RW, Kolson DL. 2000. Expression of multiple functional chemokine receptors and monocyte chemoattractant protein-1 in human neurons. Neuroscience 97:591-600.
12. Coyle DE, Li J, Baccei M. 2011. Regional differentiation of retinoic acid-induced human pluripotent embryonic carcinoma stem cell neurons. PLoS One 6:e16174.
13. Fu W, Ruangkittisakul A, Mactavish D, Shi JY, Ballanyi K, Jhamandas JH. 2012. Amyloid beta (Abeta) peptide directly activates amylin-3 receptor subtype by triggering multiple intracellular signaling pathways. J Biol Chem 287:18820-18830.
14. Gahring LC, Rogers SW. 2005. Neuronal nicotinic acetylcholine receptor expression and function on nonneuronal cells. AAPS J 7:E885-894.
15. Garcia De Arriba S, Wegner F, Gruner K, Verdaguer E, Pallas M, Camins A, Wagner A, Wohlfahrt K, Allgaier C. 2006. Different capacities of various NMDA receptor antagonists to prevent ischemia-induced neurodegeneration in human cultured NT2 neurons. Neurochem Int 49:466-474.
16. Giuliani F, Goodyer CG, Antel JP, Yong VW. 2003. Vulnerability of human neurons to T cell-mediated cytotoxicity. J Immunol 171:368-379.
17. Glaser T, Brustle O. 2005. Retinoic acid induction of ES-cell-derived neurons: the radial glia connection. Trends Neurosci 28:397-400.
18. Goodfellow CE, Graham SE, Dragunow M, Glass M. 2011. Characterization of NTera2/D1 cells as a model system for the investigation of cannabinoid function in human neurons and astrocytes. J Neurosci Res 89:1685-1697.
19. Grant SL, Shulman Y, Tibbo P, Hampson DR, Baker GB. 2006. Determination of d-serine and related neuroactive amino acids in human plasma by high-performance liquid chromatography with fluorimetric detection. J Chromatogr B Anal Technol Biomed Life Sci 844:278-282.
20. Greene LA, Tischler AS. 1976. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 73:2424-2428.
21. Guillemain I, Alonso G, Patey G, Privat A, Chaudieu I. 2000. Human NT2 neurons express a large variety of neurotransmission phenotypes in vitro. J Comp Neurol 422:380-395.
22. Guo X, Johe K, Molnar P, Davis H, Hickman J. 2010. Characterization of a human fetal spinal cord stem cell line, NSI-566RSC, and its induction to functional motoneurons. J Tissue Eng Regen Med 4:181-193.
23. + T cells are cytotoxic for human neurons. J Leukoc Biol 89:927-934.
24. Haile Y, Simmen KC, Pasichnyk D, Touret N, Simmen T, Lu JQ, Bleackley RC, Giuliani F. 2011b. Granule-derived granzyme B mediates the vulnerability of human neurons to T cell-induced neurotoxicity. J Immunol 187:4861-4872.
25. Hara K, Matsukawa N, Yasuhara T, Xu L, Yu G, Maki M, Kawase T, Hess DC, Kim SU, Borlongan CV. 2007. Transplantation of post-mitotic human neuroteratocarcinoma-overexpressing Nurr1 cells provides therapeutic benefits in experimental stroke: in vitro evidence of expedited neuronal differentiation and GDNF secretion. J Neurosci Res 85:1240-1251.
26. Hardy M, Younkin D, Tang CM, Pleasure J, Shi QY, Williams M, Pleasure D. 1994. Expression of non-NMDA glutamate receptor channel genes by clonal human neurons. J Neurochem 63:482-489.
27. Harrill JA, Freudenrich TM, Machacek DW, Stice SL, Mundy WR. 2010. Quantitative assessment of neurite outgrowth in human embryonic stem cell-derived hN2 cells using automated high-content image analysis. Neurotoxicology 31:277-290.
28. Hartley RS, Margulis M, Fishman PS, Lee VM, Tang CM. 1999. Functional synapses are formed between human NTera2 (NT2N, hNT) neurons grown on astrocytes. J Comp Neurol 407:1-10.
29. Hill EJ, Jimenez-Gonzalez C, Tarczyluk M, Nagel DA, Coleman MD, Parri HR. 2012. NT2 derived neuronal and astrocytic network signalling. PLoS One 7:e36098.
30. Ichikawa M, Matsuoka M, Mori Y. 1993. Effect of differential rearing on synapses and soma size in rat medial amygdaloid nucleus. Synapse 13:50-56.
31. Jhamandas JH, Li Z, Westaway D, Yang J, Jassar S, Mactavish D. 2011. Actions of beta-amyloid protein on human neurons are expressed through the amylin receptor. Am J Pathol 178:140-149.
32. Kernell D, Zwaagstra B. 1981. Input conductance axonal conduction velocity and cell size among hindlimb motoneurones of the cat. Brain Res 204:311-326.
33. Luessi F, Siffrin V, Zipp F. 2012. Neurodegeneration in multiple sclerosis: novel treatment strategies. Expert Rev Neurother 12:1061-1076; quiz 1077.
34. Mcewen BS. 1999. Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
35. Megiorni F, Mora B, Indovina P, Mazzilli MC. 2005. Expression of neuronal markers during NTera2/cloneD1 differentiation by cell aggregation method. Neurosci Lett 373:105-109.
36. Misiuta IE, Anderson L, Mcgrogan MP, Sanberg PR, Willing AE, Zigova T. 2003. The transcription factor Nurr1 in human NT2 cells and hNT neurons. Brain Res Dev Brain Res 145:107-115.
37. Misiuta IE, Saporta S, Sanberg PR, Zigova T, Willing AE. 2006. Influence of retinoic acid and lithium on proliferation and dopaminergic potential of human NT2 cells. J Neurosci Res 83:668-679.
38. Neelands TR, Zhang J, Macdonald RL. 1999. GABA(A) receptors expressed in undifferentiated human teratocarcinoma NT2 cells differ from those expressed by differentiated NT2-N cells. J Neurosci 19:7057-7065.
39. Newman MB, Kuo YP, Lukas RJ, Sanberg PR, Douglas Shytle R, Mcgrogan MP, Zigova T. 2002. Nicotinic acetylcholine receptors on NT2 precursor cells and hNT (NT2-N) neurons. Brain Res Dev Brain Res 139:73-86.
40. Pinto MC, De Paiva MJ, Oliveira-Lima OC, Menezes HC, Cardeal ZD, Gomez MV, Resende RR, Gomez RS. 2013. Neurochemical study of amino acids in rodent brain structures using an improved gas chromatography-mass spectrometry method. J Chem Neuroanat 7:00106-00103.
41. Pleasure SJ, Lee VM. 1993. NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J Neurosci Res 35:585-602.
42. Pleasure SJ, Page C, Lee VM. 1992. Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J Neurosci 12:1802-1815.
43. Podrygajlo G, Tegenge MA, Gierse A, Paquet-Durand F, Tan S, Bicker G, Stern M. 2009. Cellular phenotypes of human model neurons (NT2) after differentiation in aggregate culture. Cell Tissue Res 336:439-452.
44. Podrygajlo G, Song Y, Schlesinger F, Krampfl K, Bicker G. 2010. Synaptic currents and transmitter responses in human NT2 neurons differentiated in aggregate culture. Neurosci Lett 468:207-210.
45. Przyborski SA, Morton IE, Wood A, Andrews PW. 2000. Developmental regulation of neurogenesis in the pluripotent human embryonal carcinoma cell line NTERA-2. Eur J Neurosci 12:3521-3528.
46. Przyborski SA, Smith S, Wood A. 2003. Transcriptional profiling of neuronal differentiation by human embryonal carcinoma stem cells in vitro. Stem Cells 21:459-471.
47. Roep BO, Peakman M. 2010. Surrogate end points in the design of immunotherapy trials: emerging lessons from type 1 diabetes. Nat Rev Immunol 10:145-152.
48. Rosenstein JM. 1995. Diminished expression of microtubule-associated protein (MAP-2) and beta-tubulin as a putative marker for ischemic injury in neocortical transplants. Cell Transplant 4:83-91.
49. Roth TC, II, Brodin A, Smulders TV, Ladage LD, Pravosudov VV. 2010. Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus. Philos Trans R Soc Lond B Biol Sci 365:915-931.
50. Ruangkittisakul A, Schwarzacher SW, Secchia L, Poon BY, Ma Y, Funk GD, Ballanyi K. 2006. High sensitivity to neuromodulator-activated signaling pathways at physiological [K+] of confocally imaged respiratory center neurons in on-line-calibrated newborn rat brainstem slices. J Neurosci 26:11870-11880.
51. Satoh J, Kuroda Y. 2000. Differential gene expression between human neurons and neuronal progenitor cells in culture: an analysis of arrayed cDNA clones in NTera2 human embryonal carcinoma cell line as a model system. J Neurosci Methods 94:155-164.
52. Shah AJ, Crespi F, Heidbreder C. 2002. Amino acid neurotransmitters: separation approaches and diagnostic value. J Chromatogr B Anal Technol Biomed Life Sci 781:151-163.
53. Shamekh R, Cameron DF, Willing AE, Saporta S. 2006. The role of connexins in the differentiation of NT2 cells in Sertoli-NT2 cell tissue constructs grown in the rotating wall bioreactor. Exp Brain Res 170:277-284.
54. Sheridan KM, Maltese WA. 1998. Expression of Rab3A GTPase and other synaptic proteins is induced in differentiated NT2N neurons. J Mol Neurosci 10:121-128.
55. Squires PE, Wakeman JA, Chapman H, Kumpf S, Fidock MD, Andrews PW, Dunne MJ. 1996. Regulation of intracellular Ca2+ in response to muscarinic and glutamate receptor agonists during the differentiation of NTERA2 human embryonal carcinoma cells into neurons. Eur J Neurosci 8:783-793.
56. Tegenge MA, Stern M, Bicker G. 2009. Nitric oxide and cyclic nucleotide signal transduction modulates synaptic vesicle turnover in human model neurons. J Neurochem 111:1434-1446.
57. Tegenge MA, Roloff F, Bicker G. 2011. Rapid differentiation of human embryonal carcinoma stem cells (NT2) into neurons for neurite outgrowth analysis. Cell Mol Neurobiol 31:635-643.
58. van Elburg RA, van Ooyen A. 2010. Impact of dendritic size and dendritic topology on burst firing in pyramidal cells. PLoS Comput Biol 6:1000781.
59. van Pelt J, van Ooyen A. 2013. Estimating neuronal connectivity from axonal and dendritic density fields. Front Comput Neurosci 7:00160.
60. Yagita Y, Matsumoto M, Kitagawa K, Mabuchi T, Ohtsuki T, Hori M, Yanagihara T. 1999. DNA cleavage and proteolysis of microtubule-associated protein 2 after cerebral ischemia of different severity. Neuroscience 92:1417-1424.
61. Younkin DP, Tang CM, Hardy M, Reddy UR, Shi QY, Pleasure SJ, Lee VM, Pleasure D. 1993. Inducible expression of neuronal glutamate receptor channels in the NT2 human cell line. Proc Natl Acad Sci U S A 90:2174-2178.