Undifferentiated embryonic stem cells express ionotropic glutamate receptor mRNAs

Frontiers in Cellular Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Pachernegg, Svenja ^a   Joshi, Illah ^a   Muth Köhne, Elke ^a,b   Pahl, Steffen ^a   Münster, Yvonne ^a   Terhag, Jan ^a   Karus, Michael ^a,c   Werner, Markus ^a   Ma Högemeier, Zhan Lu ^a   Körber, Christoph ^a,d   Grunwald, Thomas ^a,e   Faissner, Andreas ^a   Wiese, Stefan ^a   Hollmann, Michael ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

Author keywords

Escs; Neural stem cells; Neuroepithelial cells; Patch clamp recordings; qRT PCR; Synaptic markers

Indexed keywords

AMPA RECEPTOR; BETA ACTIN; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROLIGIN 1; SYNAPSIN I; SYNAPTOBREVIN 2; SYNAPTOPHYSIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; MOUSE; NEUROTRANSMISSION; NONHUMAN; PATCH CLAMP; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 84889636335     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00241     Document Type: Article

References (47)

1. Aubert, J., Stavridis, M. P., Tweedie, S., O'reilly, M., Vierlinger, K., Li, M., et al. (2003). Screening for mammalian neural genes via fluorescenceactivated cell sorter purification of neural precursors from Sox1-gfp knockin mice. Proc. Natl. Acad. Sci. U.S.A. 100(Suppl. 1), 11836-11841. doi: 10.1073/pnas.1734197100
2. Bahn, S., Volk, B., and Wisden, W. (1994). Kainate receptor gene expression in the developing rat brain. J. Neurosci. 14, 5525-5547.
3. Bain, G., Kitchens, D., Yao, M., Huettner, J. E., and Gottlieb, D. I. (1995). Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357. doi: 10.1006/dbio.1995.1085
4. Bogen, I. L., Jensen, V., Hvalby, O., and Walaas, S. I. (2009). Synapsindependent development of glutamatergic synaptic vesicles and presynaptic plasticity in postnatal mouse brain. Neuroscience 158, 231-241. doi: 10.1016/j.neuroscience.2008.05.055
5. Brazel, C. Y., Nunez, J. L., Yang, Z., and Levison, S. W. (2005). Glutamate enhances survival and proliferation of neural progenitors derived from the subventricular zone. Neuroscience 131, 55-65. doi: 10.1016/j.neuroscience.2004.10.038
6. Cameron, H. A., McEwen, B. S., and Gould, E. (1995). Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci. 15, 4687-4692.
7. Conti, L., Pollard, S. M., Gorba, T., Reitano, E., Toselli, M., Biella, G., et al. (2005). Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 3:e283. doi: 10.1371/journal.pbio.0030283
8. Contractor, A., Sailer, A. W., Darstein, M., Maron, C., Xu, J., Swanson, G. T., et al. (2003). Loss of kainate receptor-mediated heterosynaptic facilitation of mossyfiber synapses in KA2-/mice. J. Neurosci. 23, 422-429.
9. Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D., and Malenka, R. C. (2004). Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42, 535-552. doi: 10.1016/S0896-6273(04)00266-1
10. Efroni, S., Duttagupta, R., Cheng, J., Dehghani, H., Hoeppner, D. J., Dash, C., et al. (2008). Global transcription in pluripotent embryonic stem cells. Cell Stem. Cell 2, 437-447. doi: 10.1016/j.stem.2008.03.021
11. Finley, M. F., Kulkarni, N., and Huettner, J. E. (1996). Synapse formation and establishment of neuronal polarity by P19 embryonic carcinoma cells and embryonic stem cells. J. Neurosci. 16, 1056-1065.
12. Gangaraju, V. K., and Lin, H. (2009). MicroRNAs: key regulators of stem cells. Nat. Rev. Mol. Cell Biol. 10, 116-125. doi: 10.1038/nrm2621
13. Golan-Mashiach, M., Dazard, J. E., Gerecht-Nir, S., Amariglio, N., Fisher, T., Jacob-Hirsch, J., et al. (2005). Design principle of gene expression used by human stem cells: implication for pluripotency. FASEB J. 19, 147-149. doi: 10.1096/fj.04-2417fje
14. Haydar, T. F., Wang, F., Schwartz, M. L., and Rakic, P. (2000). Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J. Neurosci. 20, 5764-5774.
15. Hollmann, M., and Heinemann, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108. doi: 10.1146/annurev.ne.17.030194.000335
16. Houbaviy, H. B., Murray, M. F., and Sharp, P. A. (2003). Embryonic stem cellspecific MicroRNAs. Dev. Cell 5, 351-358. doi: 10.1016/S1534-5807(03)00227-2
17. Jansson, L. C., Wigren, H. K., Nordstrom, T., and Akerman, K. E. (2011). Functional alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors in differentiating embryonic neural progenitor cells. Neuroreport 22, 282-287. doi: 10.1097/WNR.0b013e3283457b34
18. Kawashima, H., Numakawa, T., Kumamaru, E., Adachi, N., Mizuno, H., Ninomiya, M., et al. (2010). Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression. Neuroscience 165, 1301-1311. doi: 10.1016/j.neuroscience.2009.11.057
19. Kim, M., Habiba, A., Doherty, J. M., Mills, J. C., Mercer, R. W., and Huettner, J. E. (2009). Regulation of mouse embryonic stem cell neural differentiation by retinoic acid. Dev. Biol. 328, 456-471. doi: 10.1016/j.ydbio.2009.02.001
20. Korber, C., Werner, M., Kott, S., Ma, Z. L., and Hollmann, M. (2007). The transmembrane AMPA receptor regulatory protein gamma 4 is a more effective modulator of AMPA receptor function than stargazin (gamma 2). J. Neurosci. 27, 8442-8447. doi: 10.1523/JNEUROSCI.0424-07.2007
21. Lerma, J. (2003). Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 4, 481-495. doi: 10.1038/nrn1118
22. Lilliu, V., Perrone-Capano, C., Pernas-Alonso, R., Diaz Trelles, R., Amato, G., Zuddas, A., et al. (2002). Ontogeny of kainate receptor gene expression in the developing rat midbrain and striatum. Brain Res. Mol. Brain Res. 104, 1-10. doi: 10.1016/S0169-328X(02)00196-1
23. Liu, X. B., Murray, K. D., and Jones, E. G. (2004). Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J. Neurosci. 24, 8885-8895. doi: 10.1523/JNEUROSCI.2476-04.2004
24. Loturco, J. J., Owens, D. F., Heath, M. J., Davis, M. B., and Kriegstein, A. R. (1995). GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287-1298. doi: 10.1016/0896-6273(95)90008-X
25. Luk, K. C., and Sadikot, A. F. (2004). Glutamate and regulation of proliferation in the developing mammalian telencephalon. Dev. Neurosci. 26, 218-228. doi: 10.1159/000082139
26. Manent, J. B., Demarque, M., Jorquera, I., Pellegrino, C., Ben-Ari, Y., Aniksztejn, L., et al. (2005). A noncanonical release of GABA and glutamate modulates neuronal migration. J. Neurosci. 25, 4755-4765. doi: 10.1523/JNEUROSCI.0553-05.2005
27. Maric, D., Liu, Q. Y., Grant, G. M., Andreadis, J. D., Hu, Q., Chang, Y. H., et al. (2000). Functional ionotropic glutamate receptors emerge during terminal cell division and early neuronal differentiation of rat neuroepithelial cells. J. Neurosci. Res. 61, 652-662. doi: 10.1002/10974547(20000915)61:6<652::AID-JNR9>3.3.CO;2-A
28. Melloni, R. H. Jr., and Degennaro, L. J. (1994). Temporal onset of synapsin I gene expression coincides with neuronal differentiation during the development of the nervous system. J. Comp. Neurol. 342, 449-462. doi: 10.1002/cne.903420311
29. Meshorer, E., and Misteli, T. (2006). Chromatin in pluripotent embryonic stem cells and differentiation. Nat. Rev. Mol. Cell Biol. 7, 540-546. doi: 10.1038/nrm1938
30. Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., and Seeburg, P. H. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540. doi: 10.1016/08966273(94)90210-0
31. Monyer, H., Seeburg, P. H., and Wisden, W. (1991). Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 6, 799-810. doi: 10.1016/0896-6273(91)90176-Z
32. Mulle, C., Sailer, A., Perez-Otano, I., Dickinson-Anson, H., Castillo, P. E., Bureau, I., et al. (1998). Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392, 601-605. doi:10.1038/33408
33. Muth-Kohne, E., Pachernegg, S., Karus, M., Faissner, A., and Hollmann, M. (2010a). Expression of NMDA receptors and Ca2+-impermeable AMPA receptors requires neuronal differentiation and allows discrimination between two different types of neural stem cells. Cell. Physiol. Biochem. 26, 935-946. doi: 10.1159/000324002
34. Muth-Kohne, E., Terhag, J., Pahl, S., Werner, M., Joshi, I., and Hollmann, M. (2010b). Functional excitatory GABAA receptors precede ionotropic glutamate receptors in radial glia-like neural stem cells. Mol. Cell. Neurosci. 43, 209-221. doi: 10.1016/j.mcn.2009.11.002
35. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res. 29, e45. doi: 10.1093/nar/29.9.e45
36. Ritter, L. M., Vazquez, D. M., and Meador-Woodruff, J. H. (2002). Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Brain Res. Dev. Brain Res. 139, 227-236. doi: 10.1016/S0165-3806(02)00572-2
37. Rosa, A., and Brivanlou, A. H. (2009). microRNAs in early vertebrate development. Cell Cycle 8, 3513-3520. doi: 10.4161/cc.8.21.9847
38. Rosa, A., and Brivanlou, A. H. (2013). Regulatory non-coding RNAs in pluripotent stem cells. Int. J. Mol. Sci. 14, 14346-14373. doi: 10.3390/ijms140714346
39. Scherer, S. E., and Gallo, V. (1998). Expression and regulation of kainate and AMPA receptors in the rat neural tube. J. Neurosci. Res. 52, 356-368. doi: 10.1002/(SICI)1097-4547(19980501)52:3<356::AID-JNR12>3.3.CO;2-I
40. Schlett, K. (2006). Glutamate as a modulator of embryonic and adult neurogenesis. Curr. Top. Med. Chem. 6, 949-960. doi: 10.2174/156802606777323665
41. Sperger, J. M., Chen, X., Draper, J. S., Antosiewicz, J. E., Chon, C. H., Jones, S. B., et al. (2003). Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors. Proc. Natl. Acad. Sci. U.S.A. 100, 13350-13355. doi: 10.1073/pnas.2235735100
42. Vasileva, M., Horstmann, H., Geumann, C., Gitler, D., and Kuner, T. (2012). Synapsin-dependent reserve pool of synaptic vesicles supports replenishment of the readily releasable pool under intense synaptic transmission. Eur. J. Neurosci. 36, 3005-3020. doi: 10.1111/j.1460-9568.2012.08225.x
43. Wang, Y., Keys, D. N., Au-Young, J. K., and Chen, C. (2009). MicroRNAs in embryonic stem cells. J. Cell. Physiol. 218, 251-255. doi: 10.1002/jcp.21607
44. Yang, D., Li, T., Wang, Y., Tang, Y., Cui, H., Zhang, X., et al. (2012). miR-132 regulates the differentiation of dopamine neurons by directly targeting Nurr1 expression. J. Cell. Sci. 125, 1673-1682. doi: 10.1242/jcs.086421
45. Ying, Q. L., and Smith, A. G. (2003). Defined conditions for neural commitment and differentiation. Meth. Enzymol. 365, 327-341. doi: 10.1016/S00766879(03)65023-8
46. Ying, Q. L., Stavridis, M., Griffiths, D., Li, M., and Smith, A. (2003). Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21, 183-186. doi: 10.1038/nbt780
47. Zurmohle, U. M., Herms, J., Schlingensiepen, R., Schlingensiepen, K. H., and Brysch, W. (1994). Changes of synapsin I messenger RNA expression during rat brain development. Exp. Brain Res. 99, 17-24. doi: 10.1007/BF00241408