In Vivo synaptic scaling is mediated by GluA2-lacking AMPA receptors in the embryonic spinal cord

Journal of Neuroscience

Volumn 33, Issue 16, 2013, Pages 6791-6799

  Garcia Bereguiain, Miguel Angel ^a   Gonzalez Islas, Carlos ^a   Lindsly, Casie ^a   Butler, Ellie ^a   Hill, Atlantis Wilkins ^a   Wenner, Peter ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL) PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; LIDOCAINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HOMEOSTATIC SYNAPTIC SCALING; IMMUNOBLOTTING; IN VIVO STUDY; MINIATURE ENDPLATE POTENTIAL; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPIKE WAVE; SPINAL CORD; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP; WESTERN BLOTTING;

ANESTHETICS, LOCAL; ANIMALS; BIOPHYSICS; CHICK EMBRYO; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIDOCAINE; MOTOR NEURONS; PATCH-CLAMP TECHNIQUES; PYRIDAZINES; RECEPTORS, AMPA; SPINAL CORD; SYNAPSES; TETRODOTOXIN;

EID: 84876264783     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4025-12.2013     Document Type: Article

References (43)

1. Anggono V, Clem RL, Huganir RL (2011) PICK1 loss of function occludes homeostatic synaptic scaling. J Neurosci 31:2188-2196.
2. Aoto J, Nam CI, Poon MM, Ting P, Chen L (2008) Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 60:308-320.
3. Beique JC, Na Y, Kuhl D, Worley PF, Huganir RL (2011) Arc-dependent synapse-specific homeostatic plasticity. Proc Natl Acad Sci USA 108: 816-821.
4. Blankenship AG, Feller MB (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11:18-29.
5. Bowie D, Mayer ML (1995) Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15:453-462.
6. Cingolani LA, Thalhammer A, Yu LM, Catalano M, Ramos T, Colicos MA, GodaY (2008) Activity-dependent regulation of synaptic AMPA receptor composition and abundance by /33 integrins. Neuron 58:749-762.
7. Donevan SD, Rogawski MA (1995) Intracellular polyamines mediate inward rectification of Ca(2 +)-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Proc Natl Acad Sci USA 92:9298-9302.
8. Gainey MA, Hurvitz-Wolff JR, Lambo ME, Turrigiano GG (2009) Synaptic scaling requires the GluR2 subunit of the AMPA receptor. J Neurosci 29:6479-6489.
9. Goel A, Jiang B, Xu LW, Song L, Kirkwood A, Lee HK (2006) Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience. Nat Neurosci 9:1001-1003.
10. Goel A, Xu LW, Snyder KP, Song L, Goenaga-Vazquez Y, Megill A, Takamiya K, Huganir RL, Lee HK (2011) Phosphorylation of AMPA receptors is required for sensory deprivation-induced homeostatic synaptic plasticity. PLoS One 6:e18264.
11. Gonzalez-Islas C, Wenner P (2006) Spontaneous network activity in the embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength. Neuron 49:563-575.
12. Gonzalez-Islas C, Chub N, Wenner P (2009) NKCC1 and AE3 appear to accumulate chloride in embryonic motoneurons. J Neurophysiol 101: 507-518.
13. Gonzalez-Islas C, Chub N, Garcia-Bereguiain MA, Wenner P (2010) GABAergic synaptic scaling in embryonic motoneurons is mediated by a shift in the chloride reversal potential. J Neurosci 30:13016-13020.
14. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the normal chick embryo: 1951. Dev Dyn 195:231-272.
15. He K, Petrus E, Gammon N, Lee HK (2012) Distinct sensory requirements for unimodal and cross-modal homeostatic synaptic plasticity. J Neurosci 32:8469-8474.
16. 2+ permeability of KAAMPA-gated glutamate receptor channels depends on subunit composition. Science 252:851-853.
17. Hou Q, Zhang D, Jarzylo L, Huganir RL, Man HY (2008) Homeostatic regulation of AMPA receptor expression at single hippocampal synapses. Proc Natl Acad Sci USA 105:775-780.
18. Ibata K, Sun Q, Turrigiano GG (2008) Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 57:819-826.
19. Jakawich SK, Nasser HB, Strong MJ, McCartney AJ, Perez AS, Rakesh N, Carruthers CJ, Sutton MA (2010) Local presynaptic activity gates homeostatic changes in presynaptic function driven by dendritic BDNF synthesis. Neuron 68:1143-1158.
20. Ju W, Morishita W, Tsui J, Gaietta G, Deerinck TJ, Adams SR, Garner CC, Tsien RY, Ellisman MH, Malenka RC (2004) Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat Neu-rosci 7:244-253.
21. Koike M, Iino M, Ozawa S (1997) Blocking effect of 1-naphthyl acetyl spermine on Ca(2 +)-permeable AMPA receptors in cultured rat hippocampal neurons. Neurosci Res 29:27-36.
22. Lazzaro JT, Paternain AV, Lerma J, Chenard BL, Ewing FE, Huang J, Welch WM, Ganong AH, Menniti FS (2002) Functional characterization of CP-465,022, a selective, noncompetitive AMPA receptor antagonist. Neuropharmacology 42:143-153.
23. Lee HK (2012) Ca-permeable AMPA receptors in homeostatic synaptic plasticity. Front Mol Neurosci 5:17.
24. Man HY (2011) GluA2-lacking, calcium-permeable AMPA receptors: inducers of plasticity? Curr Opin Neurobiol 21:291-298.
25. Ni X, Sullivan GJ, Martin-Caraballo M (2007) Developmental characteristics of AMPA receptors in chick lumbar motoneurons. Dev Neurobiol 67:1419-1432.
26. O'Brien RJ, Kamboj S, Ehlers MD, Rosen KR, Fischbach GD, Huganir RL (1998) Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21:1067-1078.
27. O'Donovan MJ (1999) The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol 9:94-104.
28. O'Donovan MJ, Chub N, Wenner P (1998) Mechanisms of spontaneous activity in developing spinal networks. J Neurobiol 37:131-145.
29. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337-351.
30. Rich MM, Wenner P (2007) Sensing and expressing homeostatic synaptic plasticity. Trends Neurosci 30:119-125.
31. Shepherd JD (2012) Memory, plasticity and sleep: a role for calcium permeable AMPA receptors? Front Mol Neurosci 5:49.
32. Sun X, Zhao Y, Wolf ME (2005) Dopamine receptor stimulation modulates AMPA receptor synaptic insertion in prefrontal cortex neurons. J Neurosci 25:7342-7351.
33. Sutton MA, Ito HT, Cressy P, Kempf C, Woo JC, Schuman EM (2006) Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125:785-799.
34. Swanson GT, Kamboj SK, Cull-Candy SG (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17:58-69.
35. Thiagarajan TC, Lindskog M, Tsien RW (2005) Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47:725-737.
36. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405-496.
37. Turrigiano G (2012) Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harbor Perspect Biol 4:a005736.
38. Turrigiano GG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422-435.
39. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.
40. Vitureira N, Letellier M, Goda Y (2012) Homeostatic synaptic plasticity: from single synapses to neural circuits. Curr Opin Neurobiol 22:516-521.
41. Wierenga CJ, Ibata K, Turrigiano GG (2005) Postsynaptic expression of ho-meostatic plasticity at neocortical synapses. J Neurosci 25:2895-2905.
42. Wilhelm JC, Wenner P (2008) GABAA transmission is a critical step in the process of triggering homeostatic increases in quantal amplitude. Proc Natl Acad Sci U S A 105:11412-11417.
43. Wilhelm JC, Rich MM, Wenner P (2009) Compensatory changes in cellular excitability, not synaptic scaling, contribute to homeostatic recovery of embryonic network activity. Proc Natl Acad Sci U S A 106:6760-6765.