EphA4 expression promotes network activity and spine maturation in cortical neuronal cultures

Neural Development

Volumn 6, Issue 1, 2011, Pages

  Clifford, Meredith A ^a   Kanwal, Jessleen K ^a,b   Dzakpasu, Rhonda ^a   Donoghue, Maria J ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b THOMAS JEFFERSON HIGH SCHOOL FOR SCIENCE AND TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN RECEPTOR A4; GREEN FLUORESCENT PROTEIN;

ACTION POTENTIAL; ANIMAL; ANIMAL EMBRYO; ARTICLE; BRAIN CORTEX; CELL CULTURE; CELL DIFFERENTIATION; CERCOPITHECUS; CYTOLOGY; DENDRITIC SPINE; ELECTROPHYSIOLOGY; ELECTROPORATION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; METHODOLOGY; MOUSE; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; TIME;

ACTION POTENTIALS; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CEREBRAL CORTEX; DENDRITIC SPINES; ELECTROPHYSIOLOGY; ELECTROPORATION; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MICE; NERVE NET; NEURONS; RECEPTOR, EPHA4; TIME FACTORS; TRANSFECTION;

EID: 79955504203     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-6-21     Document Type: Article

References (63)

1. Wong RO, Meister M, Shatz CJ. Transient period of correlated bursting activity during development of the mammalian retina. Neuron 1993, 11:923-938. 10.1016/0896-6273(93)90122-8, 8240814.
2. Hanson MG, Landmesser LT. Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J Neurosci 2003, 23:587-600.
3. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 1989, 416:303-325. 1189216, 2575165.
4. Schwartz TH, Rabinowitz D, Unni V, Kumar VS, Smetters DK, Tsiola A, Yuste R. Networks of coactive neurons in developing layer 1. Neuron 1998, 20:541-552. 10.1016/S0896-6273(00)80993-9, 9539127.
5. Compte A, Reig R, Descalzo VF, Harvey MA, Puccini GD, Sanchez-Vives MV. Spontaneous high-frequency (10-80 Hz) oscillations during up states in the cerebral cortex in vitro. J Neurosci 2008, 28:13828-13844. 10.1523/JNEUROSCI.2684-08.2008, 19091973.
6. Wong RO. Retinal waves and visual system development. Annu Rev Neurosci 1999, 22:29-47. 10.1146/annurev.neuro.22.1.29, 10202531.
7. Torborg CL, Hansen KA, Feller MB. High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nat Neurosci 2005, 8:72-78. 10.1038/nn1376, 1463890, 15608630.
8. Ruthazer ES, Cline HT. Insights into activity-dependent map formation from the retinotectal system: a middle-of-the-brain perspective. J Neurobiol 2004, 59:134-146. 10.1002/neu.10344, 15007832.
9. Katz LC, Shatz CJ. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138. 10.1126/science.274.5290.1133, 8895456.
10. Wang Q, Zheng JQ. cAMP-mediated regulation of neurotrophin-induced collapse of nerve growth cones. J Neurosci 1998, 18:4973-4984.
11. Eglen SJ, Demas J, Wong RO. Mapping by waves. Patterned spontaneous activity regulates retinotopic map refinement. Neuron 2003, 40:1053-1055. 10.1016/S0896-6273(03)00808-0, 14687538.
12. Blankenship AG, Feller MB. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 2010, 11:18-29. 10.1038/nrn2759, 2902252, 19953103.
13. Catalano SM, Chang CK, Shatz CJ. Activity-dependent regulation of NMDAR1 immunoreactivity in the developing visual cortex. J Neurosci 1997, 17:8376-8390.
14. Khazipov R, Luhmann HJ. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci 2006, 29:414-418. 10.1016/j.tins.2006.05.007, 16713634.
15. Wagenaar DA, Pine J, Potter SM. An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neurosci 2006, 7:11. 10.1186/1471-2202-7-11, 1420316, 16464257.
16. Wang XJ. Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90:1195-1268.
17. Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ. Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 2006, 439:79-83. 10.1038/nature04264, 16327778.
18. le Feber J, van Pelt J, Rutten W. Latency-related development of functional connections in cultured cortical networks. Biophys J 2009, 96:3443-3450. 10.1016/j.bpj.2009.01.013, 2718268, 19383487.
19. Vajda I, van Pelt J, Wolters P, Chiappalone M, Martinoia S, van Someren E, van Ooyen A. Low-frequency stimulation induces stable transitions in stereotypical activity in cortical networks. Biophys J 2008, 94:5028-5039. 10.1529/biophysj.107.112730, 2397369, 18339760.
20. Bologna L, Nieus T, Tedesco M, Chiappalone M, Benfenati F, Martinoia S. Low-frequency stimulation enhances burst activity in cortical cultures during development. Neuroscience 2010, 165:692-704. 10.1016/j.neuroscience.2009.11.018, 19922773.
21. Chiappalone M, Casagrande S, Tedesco M, Valtorta F, Baldelli P, Martinoia S, Benfenati F. Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I-deficient cortical networks. Cereb Cortex 2009, 19:1422-1439. 10.1093/cercor/bhn182, 19020204.
22. Chiappalone M, Massobrio P, Martinoia S. Network plasticity in cortical assemblies. Eur J Neurosci 2008, 28:221-237. 10.1111/j.1460-9568.2008.06259.x, 18662344.
23. Xing W-L, Cheng J. Frontiers in Biochip Technology 2006, New York: Springer.
24. Segev R, Benveniste M, Shapira Y, Ben-Jacob E. Formation of electrically active clusterized neural networks. Phys Rev Lett 2003, 90:168101.
25. Hulata E, Baruchi I, Segev R, Shapira Y, Ben-Jacob E. Self-regulated complexity in cultured neuronal networks. Phys Rev Lett 2004, 92:198105.
26. Chiappalone M, Vato A, Tedesco MB, Marcoli M, Davide F, Martinoia S. Networks of neurons coupled to microelectrode arrays: a neuronal sensory system for pharmacological applications. Biosens Bioelectron 2003, 18:627-634. 10.1016/S0956-5663(03)00041-1, 12706572.
27. Petermann T, Thiagarajan TC, Lebedev MA, Nicolelis MA, Chialvo DR, Plenz D. Spontaneous cortical activity in awake monkeys composed of neuronal avalanches. Proc Natl Acad Sci USA 2009, 106:15921-15926. 10.1073/pnas.0904089106, 2732708, 19717463.
28. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998, 391:892-896. 10.1038/36103, 9495341.
29. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG, Pawson T, Davis S, Yancopoulos GD. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 1996, 17:9-19. 10.1016/S0896-6273(00)80276-7, 8755474.
30. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008, 133:38-52. 10.1016/j.cell.2008.03.011, 18394988.
31. Holland SJ, Gale NW, Mbamalu G, Yancopoulos GD, Henkemeyer M, Pawson T. Bidirectional signalling through the Eph-family receptor Nuk and its transmembrane ligands. Nature 1996, 383:722. 10.1038/383722a0, 8878483.
32. Cowan CA, Henkemeyer M. Ephrins in reverse, park and drive. Trends Cell Biol 2002, 12:339-346. 10.1016/S0962-8924(02)02317-6, 12185851.
33. Davy A, Aubin J, Soriano P. Ephrin-B1 forward and reverse signaling are required during mouse development. Genes Dev 2004, 18:572-583. 10.1101/gad.1171704, 374238, 15037550.
34. Davy A, Soriano P. Ephrin signaling in vivo: look both ways. Dev Dyn 2005, 232:1-10. 10.1002/dvdy.20200, 15580616.
35. Gale NW, Yancopoulos GD. Ephrins and Their receptors: a repulsive topic?. Cell Tissue Res 1997, 290:227-241. 10.1007/s004410050927, 9321684.
36. Hansen MJ, Dallal GE, Flanagan JG. Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 2004, 42:717-730. 10.1016/j.neuron.2004.05.009, 15182713.
37. Brown A, Yates PA, Burrola P, Ortuno D, Vaidya A, Jessell TM, Pfaff SL, O'Leary DD, Lemke G. Topographic mapping from the retina to the midbrain is controlled by relative but not absolute levels of EphA receptor signaling. Cell 2000, 102:77-88. 10.1016/S0092-8674(00)00012-X, 10929715.
38. Yokote H, Fujita K, Jing X, Sawada T, Liang S, Yao L, Yan X, Zhang Y, Schlessinger J, Sakaguchi K. Trans-activation of EphA4 and FGF receptors mediated by direct interactions between their cytoplasmic domains. Proc Natl Acad Sci USA 2005, 102:18866-18871. 10.1073/pnas.0509741102, 1323220, 16365308.
39. Yun ME, Johnson RR, Antic A, Donoghue MJ. EphA family gene expression in the developing mouse neocortex: regional patterns reveal intrinsic programs and extrinsic influence. J Comp Neurol 2003, 456:203-216. 10.1002/cne.10498, 12528186.
40. North HA, Zhao X, Kolk SM, Clifford MA, Ziskind DM, Donoghue MJ. Promotion of proliferation in the developing cerebral cortex by EphA4 forward signaling. Development 2009, 136:2467-2476. 10.1242/dev.034405, 2729353,2729353, 19542359.
41. Bouvier D, Corera AT, Tremblay ME, Riad M, Chagnon M, Murai KK, Pasquale EB, Fon EA, Doucet G. Pre-synaptic and post-synaptic localization of EphA4 and EphB2 in adult mouse forebrain. J Neurochem 2008, 106:682-695. 10.1111/j.1471-4159.2008.05416.x, 18410519.
42. Bouvier D, Tremblay ME, Riad M, Corera AT, Gingras D, Horn KE, Fotouhi M, Girard M, Murai KK, Kennedy TE, McPherson PS, Pasquale EB, Fon EA, Doucet G. EphA4 is localized in clathrin-coated and synaptic vesicles in adult mouse brain. J Neurochem 2010, 113:153-165. 10.1111/j.1471-4159.2010.06582.x, 20067584.
43. Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 2003, 6:153-160. 10.1038/nn994, 12496762.
44. Bourgin C, Murai KK, Richter M, Pasquale EB. The EphA4 receptor regulates dendritic spine remodeling by affecting beta1-integrin signaling pathways. J Cell Biol 2007, 178:1295-1307. 10.1083/jcb.200610139, 2064660, 17875741.
45. Inoue E, Deguchi-Tawarada M, Togawa A, Matsui C, Arita K, Katahira-Tayama S, Sato T, Yamauchi E, Oda Y, Takai Y. Synaptic activity prompts gamma-secretase-mediated cleavage of EphA4 and dendritic spine formation. J Cell Biol 2009, 185:551-564. 10.1083/jcb.200809151, 2700400, 19414612.
46. Filosa A, Paixao S, Honsek SD, Carmona MA, Becker L, Feddersen B, Gaitanos L, Rudhard Y, Schoepfer R, Klopstock T, Kullander K, Rose CR, Pasquale EB, Klein R. Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nat Neurosci 2009, 12:1285-1292. 10.1038/nn.2394, 19734893.
47. Grunwald IC, Korte M, Adelmann G, Plueck A, Kullander K, Adams RH, Frotscher M, Bonhoeffer T, Klein R. Hippocampal plasticity requires postsynaptic ephrinBs. Nat Neurosci 2004, 7:33-40. 10.1038/nn1164, 14699416.
48. Fu AK, Hung KW, Fu WY, Shen C, Chen Y, Xia J, Lai KO, Ip NY. APC(Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity. Nat Neurosci 2011, 14:181-9. 10.1038/nn.2715, 21186356.
49. Kamioka H, Maeda E, Jimbo Y, Robinson HP, Kawana A. Spontaneous periodic synchronized bursting during formation of mature patterns of connections in cortical cultures. Neurosci Lett 1996, 206:109-112. 10.1016/S0304-3940(96)12448-4, 8710163.
50. Shew WL, Yang H, Petermann T, Roy R, Plenz D. Neuronal avalanches imply maximum dynamic range in cortical networks at criticality. J Neurosci 2009, 29:15595-15600. 10.1523/JNEUROSCI.3864-09.2009, 20007483.
51. Takayama Y, Moriguchi H, Kotani K, Jimbo Y. Spontaneous calcium transients in cultured cortical networks during development. IEEE Trans Biomed Eng 2009, 56:2949-2956.
52. Sernagor E, Grzywacz NM. Spontaneous activity in developing turtle retinal ganglion cells: pharmacological studies. J Neurosci 1999, 19:3874-3887.
53. Yuste R, Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001, 24:1071-1089. 10.1146/annurev.neuro.24.1.1071, 11520928.
54. Gullo F, Mazzetti S, Maffezzoli A, Dossi E, Lecchi M, Amadeo A, Krajewski J, Wanke E. Orchestration of "presto" and "largo" synchrony in up-down activity of cortical networks. Front Neural Circuits 2010, 4:11. 2866559, 20461235.
55. Irwin SA, Galvez R, Greenough WT. Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb Cortex 2000, 10:1038-1044. 10.1093/cercor/10.10.1038, 11007554.
56. Dufour A, Seibt J, Passante L, Depaepe V, Ciossek T, Frisen J, Kullander K, Flanagan JG, Polleux F, Vanderhaeghen P. Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron 2003, 39:453-465. 10.1016/S0896-6273(03)00440-9, 12895420.
57. Houweling AR, Brecht M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 2008, 451:65-68. 10.1038/nature06447, 18094684.
58. Wolfe J, Houweling AR, Brecht M. Sparse and powerful cortical spikes. Curr Opin Neurobiol 20:306-312.
59. Voigt BC, Brecht M, Houweling AR. Behavioral detectability of single-cell stimulation in the ventral posterior medial nucleus of the thalamus. J Neurosci 2008, 28:12362-12367. 10.1523/JNEUROSCI.3046-08.2008, 19020029.
60. Brecht M, Schneider M, Sakmann B, Margrie TW. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 2004, 427:704-710. 10.1038/nature02266, 14973477.
61. Li CY, Poo MM, Dan Y. Burst spiking of a single cortical neuron modifies global brain state. Science 2009, 324:643-646. 10.1126/science.1169957, 2913066, 19407203.
62. Brewer GJ, Boehler MD, Pearson RA, DeMaris AA, Ide AN, Wheeler BC. Neuron network activity scales exponentially with synapse density. J Neural Eng 2009, 6:014001. 10.1088/1741-2560/6/1/014001, 2679226, 19104141.
63. Fischer M, Kaech S, Knutti D, Matus A. Rapid actin-based plasticity in dendritic spines. Neuron 1998, 20:847-854. 10.1016/S0896-6273(00)80467-5, 9620690.