Synapse formation and establishment of neuronal polarity by P19 embryonic carcinoma cells and embryonic stem cells

Journal of Neuroscience

Volumn 16, Issue 3, 1996, Pages 1056-1065

  Finley, Michael F A ^a   Kulkarni, Nita ^a   Huettner, James E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

embryonic carcinoma cells; embryonic stem cells; neuronal differentiation; neuronal polarity; NMDA receptors; synaptic transmission

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLYCINE RECEPTOR; MICROTUBULE ASSOCIATED PROTEIN 2; MONOCLONAL ANTIBODY; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROMODULIN; SYNAPSIN;

ANIMAL CELL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CANCER CELL CULTURE; CENTRAL NERVOUS SYSTEM; EMBRYO; EMBRYONAL CARCINOMA; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; STEM CELL; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

EID: 0029985691     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-03-01056.1996     Document Type: Article

References (66)

1. Andrews PW (1984) Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol 103:285-293.
2. Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI (1995) Embryonic stem cells express neuronal properties in vitro. Dev Biol 168:342-357.
3. Bain G, Ramkumar TP, Cheng JM, Gottlieb DI (1993) Expression of the genes coding for glutamic acid decarboxylase in pluripotent cell lines. Mol Brain Res 17:23-30.
4. Barker J, Harrison NL (1988) Outward rectification of inhibitory postsynaptic currents in cultured rat hippocampal neurones. J Physiol (Lond) 403:41-55.
5. Bekkers JM, Stevens CF (1989) NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus. Nature 341:230-233.
6. Bekkers JM, Richerson GB, Stevens CF (1990) Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc Natl Acad Sci USA 87:5359-5362.
7. Bormann J, Hamil OP, Sakmann B (1987) Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurones. J Physiol (Lond) 385:243-286.
8. Buckley K, Kelly RB (1985) Identification of a transmembrane glycoprotein specific for secretory vesicles of neuronal and endocrine cells. J Cell Biol 100:1284-1294.
9. Capecchi MR (1989) Altering the genome by homologous recombination. Science 244:1288-1292.
10. Cepko C (1988) Immortalization of neural cells via oncogene transduction. Trends Neurosci 11:6-8.
11. Craig AM, Banker G (1994) Neuronal polarity. Annu Rev Neurosci 17:267-310.
12. Dinsmore JH, Solomon F (1991) Inhibition of MAP2 expression affects both morphological and cell division phenotypes of neuronal differentiation. Cell 64:817-826.
13. Edwards FA, Konnerth A, Sakmann B (1990) Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J Physiol (Lond) 430:213-249.
14. Fischbach GD, Nelson PG (1977) Cell culture in neurobiology. In: Handbook of physiology, Sect 1, The nervous system (Kandel ER, ed), pp 719-774. Bethesda: American Physiological Society.
15. Fishell G (1995) Striatal precursors adopt cortical identities in response to local cues. Development 121:803-812.
16. Fletcher TL, Cameron P, De Camilli P, Banker G (1991) The distribution of synapsin 1 and synaptophysin in hippocampal neurons developing in culture. J Neurosci 11:1617-1626.
17. Forsythe ID, Westbrook GL (1988) Slow excitatory postsynaptic currents mediated by N-methyl-D-aspartate receptors on cultured mouse central neurones. J Physiol (Lond) 396:515-533.
18. Gage FH, Ray J, Fisher LJ (1995) Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 18:159-192.
19. Galileo DS, Gray GE, Owens GC, Majors J, Sanes JR (1990) Neurons and glia arise from a common progenitor in chick optic tectum: demonstration with two retroviruses and cell type-specific antibodies. Proc Natl Acad Sci USA 87:458-462.
20. Goslin K, Schreyer DJ, Skene JHP, Banker G (1990) Changes in the distribution of GAP-43 during the development of neuronal polarity. J Neurosci 10:588-602.
21. A mRNA have functional receptors. J Neurosci 14:5429-5436.
22. Hestrin S (1992) Activation and desensitization of glutamate-activated channels mediating fast excitatory synaptic currents in the visual cortex. Neuron 9:991-999.
23. Hestrin S, Nicoll RA, Perkel DJ, Sah P (1990) Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol (Lond) 422:203-225.
24. Huettner JE, Baughman RW (1986) Primary culture of identified neurons from the visual cortex of postnatal rats. J Neurosci 6:3044-3060.
25. Huettner JE, Baughman RW (1988) The pharmacology of synapses formed by identified corticocollicular neurons in primary cultures of rat visual cortex. J Neurosci 8:160-175.
26. Jahn R, Schiebler W, Ouimet C, Greengard P (1985) A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci USA 82:4137-4141.
27. Jonas P, Major G, Sakmann B (1993) Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol (Lond) 472:615-663.
28. Jones-Villeneuve EMV, McBurney MW, Rogers KA, Kalnins VI (1982) Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J Cell Biol 94:253-262.
29. Jones-Villeneuve EMV, Rudnicki MA, Harris JF, McBurney MW (1983) Retinoic acid-induced neural differentiation of embryonal carcinoma cells. Mol Cell Biol 3:2271-2279.
30. Kleppner SR, Robinson KA, Trojanowski JQ, Lee VM-Y (1995) Transplanted human neurons derived from a teratocarcinoma cell line (NTera-2) mature, integrate, and survive for over 1 year in the nude mouse brain. J Comp Neurol 357:618-632.
31. Krupp J, Feltz P (1993) Synaptic- and agonist-induced chloride currents in neonatal rat sympathetic preganglionic neurones. J Physiol (Lond) 471:729-748.
32. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404.
33. Liu G, Tsien RW (1995) Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375:404-408.
34. LoPresti P, Poluha W, Poluha DK, Drinkwater E, Ross AH (1992) Neuronal differentiation triggered by blocking cell proliferation. Cell Growth Differ 3:627-635.
35. Magnuson DSK, Morassutti DJ, Staines WA, McBurney MW, Marshall KC (1995) In vivo electrophysiological maturation of neurons derived from a multipotent precursor (embryonal carcinoma) cell line. Dev Brain Res 84:130-141.
36. McBurney MW, Reuhl KR, Ally AI, Nasipuri S, Bell JC, Craig J (1988) Differentiation and maturation of embryonal carcinoma-derived neurons in cell culture. J Neurosci 8:1063-1073.
37. Meiri KF, Pfenninger KH, Willard MB (1986) Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc Natl Acad Sci USA 83:3537-3541.
38. Meiri KF, Willard M, Johnson MI (1988) Distribution and phosphorylation of the growth-associated protein GAP-43 in regenerating sympathetic neurons in culture. J Neurosci 8:2571-2581.
39. Mennerick S, Que J, Benz A, Zorumski CF (1995) Passive and synaptic properties of hippocampal neurons grown in microcultures and mass cultures. J Neurophysiol 73:320-332.
40. Nelson PG (1976) Central nervous system synapses in cell culture. Cold Spring Harb Symp Quant Biol 40:359-371.
41. Nelson PG, Christian C, Nirenberg M (1976) Synapse formation between clonal neuroblastoma X glioma hybrid cells and striated muscle cells. Proc Natl Acad Sci USA 73:123-127.
42. Nirenberg M, Wilson SP, Higashida H, Rotter A, Kreuger K, Busis N, Ray R, Kenimer J, Adler M, Fukui H (1983) Synapse formation by neuroblastoma hybrid cells. Cold Spring Harb Symp Quant Biol 48:707-715
43. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-465.
44. Pleasure SJ, Page C, Lee VM-Y (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.
45. Price J, Turner D, Cepko C (1987) Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc Natl Acad Sci USA 84:156-160.
46. Renfranz PJ, Cunningham MG, McKay RDG (1991) Region-specific differentiation of the hippocampal stem cell line HiB5 upon implantation into the developing mammalian brain. Cell 66:713-729.
47. Ryder EF, Snyder EY, Cepko CL (1990) Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J Neurobiol 21:356-375.
48. Schubert D, Heinemann S, Carlisle W, Tarikas H, Kimes B, Patrick J, Steinbach J H, Culp W, Brandt BL (1974) Clonal cell lines from the rat central nervous system. Nature 249:224-227.
49. Schubert D, Heinemann S, Kidokoro Y (1977) Cholinergic metabolism and synapse formation by a rat nerve cell line. Proc Natl Acad Sci USA 74:2579-2583
50. Segal MM, Furshpan EJ (1990) Epileptiform activity in microcultures containing small numbers of hippocampal neurons. J Neurophysiol 64:1390-1399.
51. Shirasaki T, Klee MR, Nakaye T, Akaike N (1991) Differential blockade of bicuculline and strychnine on GABA- and glycine-induced responses in dissociated rat hippocampal pyramidal cells. Brain Res 561:77-83.
52. Skene JHP, Willard M (1981) Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. J Cell Biol 89:96-103.
53. Sloboda RD, Rudolph SA, Rosenbaum JL, Greengard P (1975) Cyclic AMP-dependent endogenous phosphorylation of a microtubial-associated protein. Proc Natl Acad Sci USA 72:177-181.
54. Snyder EY, Deitcher DL, Walsh C, Arnold-Aldea S, Hartwieg EA, Cepko CL (1992) Multiple neural cell lines can engraft and participate in development of mouse cerebellum. Cell 68:33-51.
55. Sommer B, Kohler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11-19.
56. Staines WA, Morassutti DJ, Reuhl KR, Ally AI, McBurney MW (1994) Neurons derived from P19 embryonal carcinoma cells have varied morphologies and neurotransmitters. Neuroscience 58:735-751.
57. Sucher NJ, Brose N, Deitcher DL, Awobuluyi M, Gasic GP, Bading H, Cepko CL, Greenberg ME, Jahn R, Heinemann SF, Lipton SA (1993) Expression of endogenous NMDAR1 transcripts without receptor protein suggests post-transcriptional control in PC12 cells. J Biol Chem 268:22299-22304.
58. Südhof TC, Czernik AJ, Kao H-T, Taki K, Johnston PA, Horiuchi A, Kanazir SD, Wagner MA, Perin MS, De Camilli P, Greengard P (1989) Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science 245:1474-1480.
59. Takahashi T, Momiyama A, Hirai K, Hishinuma F, Akagi H (1992) Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels. Neuron 9:1155-1161.
60. Temple S (1989) Division and differentiation of isolated CNS blast cells in microculture. Nature 340:471-473.
61. Tong G, Jahr CE (1994) Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13:1195-1203.
62. Turetsky DM, Huettner JE, Gottlieb DI, Goldberg MP, Choi DW (1993) Glutamate receptor-mediated currents and toxicity in embryonal carcinoma cells. J Neurobiol 24:1157-1169.
63. Turner D, Cepko C (1987) Cell lineage in the rat retina: a common progenitor for neurons and glia persists late in development. Nature 328:131-136.
64. Weisskopf MG, Nicoll RA (1995) Presynaptic changes during mossy fibre LTP revealed by NMDA receptor-mediated synaptic responses. Nature 376:256-259.
65. r 38,000 characteristic of presynaptic vesicles. Cell 41:1017-1028.
66. Younkin DP, Tang C-M, Hardy M, Reddy UR, Shi Q-Y, Pleasure SJ, Lee VM-Y, Pleasure D (1993) Inducible expression of neuronal glutamate receptor channels in the NT2 human cell line. Proc Natl Acad Sci USA 90:2174-2178.