KCC2 gates activity-driven AMPA receptor traffic through Cofilin phosphorylation

Journal of Neuroscience

Volumn 35, Issue 48, 2015, Pages 15772-15786

  Chevy, Quentin ^a,b,c   Heubl, Martin ^a,b,c   Goutierre, Marie ^a,b,c   Backer, Stéphanie ^a   Moutkine, Imane ^a,b,c   Eugène, Emmanuel ^a,b,c   Bloch Gallego, Evelyne ^a   Lévi, Sabine ^a,b,c   Poncer, Jean Christophe ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUT DU FER À MOULIN   (France)

Author keywords

Actin; AMPA receptor; KCC2; Spine; STED microscopy; Synaptic plasticity

Indexed keywords

ACTIN; AMPA RECEPTOR; CHLORIDE ION; COFILIN; GLUTAMATE RECEPTOR 1; LENTIVIRUS VECTOR; POTASSIUM CHLORIDE COTRANSPORTER 2; ACTIN DEPOLYMERIZING FACTOR; COTRANSPORTER; DOXYCYCLINE; ENZYME INHIBITOR; N-(4-METHYLTHIAZOL-2-YL)-2-(6-PHENYLPYRIDAZIN-3-YLTHIO)ACETAMIDE; POTASSIUM-CHLORIDE SYMPORTERS; SMALL INTERFERING RNA; THIAZOLE DERIVATIVE; THIOGLYCOLIC ACID DERIVATIVE;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; FLUORESCENCE IMAGING; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GLUTAMATERGIC SYNAPSE; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MALE; MICROSCOPY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; SPINE; STIMULATED EMISSION DEPLETION MICROSCOPY; ANIMAL; ANIMAL EMBRYO; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; DENDRITIC SPINE; DOSE RESPONSE; DRUG EFFECTS; GENETICS; METABOLISM; NERVE CELL; PROTEIN TRANSPORT; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; CELLS, CULTURED; DENDRITIC SPINES; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXYCYCLINE; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; EXOCYTOSIS; HIPPOCAMPUS; NEURONS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RNA, SMALL INTERFERING; SYMPORTERS; THIAZOLES; THIOGLYCOLATES;

EID: 84949441518     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1735-15.2015     Document Type: Article

References (73)

1. Ashby MC, Maier SR, Nishimune A, Henley JM (2006) Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci 26:7046-7055. CrossRef Medline
2. Backer S, Hidalgo-Sánchez M, Offner N, Portales-Casamar E, Debant A, Fort P, Gauthier-Rouvière C, Bloch-Gallego E (2007) Trio controls the mature organization of neuronal clusters in the hindbrain. J Neurosci 27: 10323-10332. CrossRef Medline
3. Baines AJ, Lu HC, Bennett PM (2014) The Protein 4.1 family: hub proteins Chevy et al. KCC2 Gates LTP Expression at Hippocampal Synapsesin animals for organizing membrane proteins. Biochim Biophys Acta 1838:605-619. CrossRef Medline
4. Blaesse P, Airaksinen MS, Rivera C, Kaila K (2009) Cation-chloride cotransporters and neuronal function. Neuron 61:820-838. CrossRef Medline
5. Bos R, Sadlaoud K, Boulenguez P, Buttigieg D, Liabeuf S, Brocard C, Haase G, Bras H, Vinay L (2013) Activation of 5-HT2A receptors upregulates the function of the neuronal K-Cl cotransporter KCC2. Proc Natl Acad Sci SA110:348-353. CrossRefMedline
6. Bosch M, Hayashi Y (2012) Structural plasticity of dendritic spines. Curr Opin Neurobiol 22:383-388. CrossRef Medline
7. Boulenguez P, Liabeuf S, Bos R, Bras H, Jean-Xavier C, Brocard C, Stil A, Darbon P, Cattaert D, Delpire E, Marsala M, Vinay L (2010) Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 16:302-307. CrossRef Medline
8. Causeret F, Hidalgo-Sanchez M, Fort P, Backer S, Popoff MR, Gauthier-Rouvière C, Bloch-Gallego E (2004) Distinct roles of Rac1/Cdc42 and Rho/Rock for axon outgrowth and nucleokinesis of precerebellar neurons toward netrin 1. Development 131:2841-2852. CrossRef Medline
9. Chamma I, Chevy Q, Poncer JC, Lévi S (2012) Role of the neuronal K-Clcotransporter KCC2 in inhibitory and excitatory neurotransmission. Front Cell Neurosci 6:5. CrossRef Medline
10. Chamma I, Heubl M, Chevy Q, Renner M, Moutkine I, Eugène E, Poncer JC, Lévi S (2013) Activity-dependent regulation of the K/Cl transporter KCC2 membrane diffusion, clustering, and function in hippocampal neurons. J Neurosci 33:15488-15503. CrossRef Medline
11. Cingolani LA, Goda Y (2008) Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9:344-356. CrossRef Medline
12. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421. CrossRef Medline
13. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sík A, De Koninck P, De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinallamina I neurons as a mechanism of neuropathic pain. Nature 424:938-942. CrossRef Medline
14. Delpire E, Days E, Lewis LM, Mi D, Kim K, Lindsley CW, Weaver CD (2009) Small-molecule screen identifies inhibitors of the neuronal K-Cl cotransporter KCC2. Proc Natl Acad Sci U S A 106:5383-5388. CrossRef Medline
15. Dumitriu D, Rodriguez A, Morrison JH (2011) High-throughput, detailed, cell-specific neuroanatomy of dendritic spines using microinjection and confocal microscopy. Nat Protoc 6:1391-1411. CrossRef Medline
16. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143. CrossRef Medline
17. Fiumelli H, Cancedda L, Poo MM (2005) Modulation of GABAergic transmission by activity via postsynaptic Ca 2 -dependent regulation of KCC2 function. Neuron 48:773-786. CrossRef Medline
18. Fiumelli H, Briner A, Puskarjov M, Blaesse P, Belem BJ, Dayer AG, Kaila K, Martin JL, Vutskits L (2013) An ion transport-independent role for the cation-chloride cotransporter KCC2 in dendritic spinogenesis in vivo. Cereb Cortex 23:378-388. CrossRef Medline
19. Gagnon M, Bergeron MJ, Lavertu G, Castonguay A, Tripathy S, Bonin RP, Perez-Sanchez J, Boudreau D, Wang B, Dumas L, Valade I, Bachand K, Jacob-Wagner M, Tardif C, Kianicka I, Isenring P, Attardo G, Coull JA, De Koninck Y (2013) Chloride extrusion enhancers as novel therapeutics for neurological diseases. Nat Med 19:1524-1528. CrossRef Medline.
20. Gasman S, Chasserot-Golaz S, Popoff MR, Aunis D, Bader MF (1999) Involvement of Rho GTPases in calcium-regulated exocytosis from adrenal chromaffin cells. J Cell Sci 112:4763-4771. Medline
21. Gauvain G, Chamma I, Chevy Q, Cabezas C, Irinopoulou T, Bodrug N, Carnaud M, Lévi S, Poncer JC (2011) The neuronal K-Cl cotransporter KCC2 influences postsynaptic AMPA receptor content and lateral diffusion in dendritic spines. Proc Natl Acad Sci U S A 108:15474-15479. CrossRef Medline
22. Gu J, Lee CW, Fan Y, Komlos D, Tang X, Sun C, Yu K, Hartzell HC, Chen G, Bamburg JR, Zheng JQ (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci 13:1208-1215. CrossRef Medline
23. Gulyás AI, Sík A, Payne JA, Kaila K, Freund TF (2001) The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur J Neurosci 13:2205-2217. CrossRef Medline
24. Harrington WW, Britt C, Wilson J, Milliken N, Binz J, Lobe D, Oliver W, Lewis M, Ignar D (2007) The effect of PPARalpha, PPARdelta, PPAR- gamma, and PPARpan agonists on body weight, body mass, and serum lipid profiles in dietinduced obese AKR/J Mice. PPAR Res 2007:97125. CrossRef Medline
25. Harvey CD, Svoboda K (2007) Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450:1195-1200. CrossRef Medline
26. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267. CrossRef Medline
27. Huang YY, Colino A, Selig DK, Malenka RC (1992) The influence of prior synaptic activity on the induction of long-term potentiation. Science 255: 730-733. CrossRef Medline
28. Huganir RL, Nicoll RA (2013) AMPARs and synaptic plasticity: the last 25 years. Neuron 80:704-717. CrossRef Medline
29. Hyde TM, Lipska BK, Ali T, Mathew SV, Law AJ, Metitiri OE, Straub RE, Ye T, Colantuoni C, Herman MM, Bigelow LB, Weinberger DR, Kleinman JE (2011) Expression of GABA signaling molecules KCC2, NKCC1, and GAD1 in cortical development and schizophrenia. J Neurosci 31:11088-11095. CrossRef Medline
30. Ivakine EA, Acton BA, Mahadevan V, Ormond J, Tang M, Pressey JC, Huang MY, Ng D, Delpire E, Salter MW, Woodin MA, McInnes RR (2013) Neto2 is a KCC2 interacting protein required for neuronal Clregulation in hippocampal neurons. Proc Natl Acad Sci U S A 110:3561-3566. CrossRef Medline
31. Jaenisch N, Witte OW, Frahm C (2010) Downregulation of potassium chloride cotransporter KCC2 after transient focal cerebral ischemia. Stroke 41:e151-e159. CrossRef Medline
32. Jin X, Huguenard JR, Prince DA (2005) Impaired Cl extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J Neurophysiol 93:2117-2126. CrossRef Medline
33. Kahle KT, Staley KJ, Nahed BV, Gamba G, Hebert SC, Lifton RP, Mount DB (2008) Roles of the cation-chloride cotransporters in neurological disease. Nat Clin Pract Neurol 4:490-503.
34. CrossRef Medline Kahle KT, Deeb TZ, Puskarjov M, Silayeva L, Liang B, Kaila K, Moss SJ (2013) Modulation of neuronal activity by phosphorylation of the K-Cl cotransporter KCC2. Trends Neurosci 36:726-737.
35. CrossRef Medline Kato K, Li ST, Zorumski CF (1999) Modulation of long-term potentiation induction in the hippocampus by N-methyl-D-aspartate-mediated pre- synaptic inhibition. Neuroscience 92:1261-1272. CrossRef Medline
36. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26:2000-2009. CrossRef Medline
37. Kopec CD, Real E, Kessels HW, Malinow R (2007) GluR1 links structural and functional plasticity at excitatory synapses. J Neurosci 27:13706-13718. CrossRef Medline
38. Lee HH, Jurd R, Moss SJ (2010) Tyrosine phosphorylation regulates the membrane trafficking of the potassium chloride cotransporter KCC2. Mol Cell Neurosci 45:173-179. CrossRef Medline
39. Lee HH, Deeb TZ, Walker JA, Davies PA, Moss SJ (2011) NMDA receptor activity downregulates KCC2 resulting in depolarizing GABA(A) receptor-mediated currents. Nat Neurosci 14:736-743. CrossRef Medline
40. Li H, Khirug S, Cai C, Ludwig A, Blaesse P, Kolikova J, Afzalov R, Coleman SK, Lauri S, Airaksinen MS, Keinänen K, Khiroug L, Saarma M, Kaila K, Rivera C (2007) KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron 56:1019-1033. CrossRef Medline
41. Lin DT, Makino Y, Sharma K, Hayashi T, Neve R, Takamiya K, Huganir RL (2009) Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat Neurosci 12:879-887. CrossRef Medline
42. Llano O, Smirnov S, Soni S, Golubtsov A, Guillemin I, Hotulainen P, Medina I, Nothwang HG, Rivera C, Ludwig A (2015) KCC2 regulates actin dynamics in dendritic spines via interaction with beta-PIX. J Cell Biol 209: 671-686. CrossRef Medline
43. Löscher W, Puskarjov M, Kaila K (2013) Cation-chloride cotransporters NKCC1 and KCC2 as potential targets for novel antiepileptic and antiepileptogenic treatments. Neuropharmacology 69:62-74. CrossRef Medline
44. Mahadevan V, Pressey JC, Acton BA, Uvarov P, Huang MY, Chevrier J, Puchalski A, Li CM, Ivakine EA, Airaksinen MS, Delpire E, McInnes RR, Woodin MA (2014) Kainate receptors coexist in a functional complex with KCC2 and regulate chloride homeostasis in hippocampal neurons. Cell Rep 7:1762-1770. CrossRef Medline
45. Makino H, Malinow R (2011) Compartmentalized versus global synaptic plasticity on dendrites controlled by experience. Neuron 72:1001-1011. CrossRef Medline
46. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126. CrossRef Medline
47. Medina I, Friedel P, Rivera C, Kahle KT, Kourdougli N, Uvarov P, Pellegrino C (2014) Current view on the functional regulation of the neuronal K(+)-Cl(-) cotransporter KCC2. Front Cell Neurosci 8:27. CrossRef Medline
48. Miles R, Blaesse P, Huberfeld G, Wittner L, Kaila K (2012) Chloride homeostasis and GABA signaling in temporal lobe epilepsy. In: Jasper’s basic mechanisms of the epilepsies (Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, eds). Bethesda, MD: National Center for Biotechnology Information.
49. Moran PA (1948) The interpretation of statistical maps. J R Stat Soc Series B 10:243-251.
50. Okamoto K, Nagai T, Miyawaki A, Hayashi Y (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112. CrossRef Medline
51. Otmakhov N, Tao-Cheng JH, Carpenter S, Asrican B, Dosemeci A, Reese TS, Lisman J (2004) Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation. J Neurosci 24: 9324-9331. CrossRef Medline
52. Ouyang Y, Wong M, Capani F, Rensing N, Lee CS, Liu Q, Neusch C, Martone ME, Wu JY, Yamada K, Ellisman MH, Choi DW (2005) Transient decrease in Factin may be necessary for translocation of proteins into dendritic spines. Eur J Neurosci 22:2995-3005. CrossRef Medline
53. Pallud J, Le Van Quyen M, Bielle F, Pellegrino C, Varlet P, Labussiere M, Cresto N, Dieme MJ, Baulac M, Duyckaerts C, Kourdougli N, Chazal G, Devaux B, Rivera C, Miles R, Capelle L, Huberfeld G (2014) Cortical GABAergic excitation contributes to epileptic activities around human glioma. Sci Transl Med 6:244ra289. CrossRef Medline
54. Park E, Na M, Choi J, Kim S, Lee JR, Yoon J, Park D, Sheng M, Kim E (2003) The Shank family of postsynaptic density proteins interacts with and promotes synaptic accumulation of the beta PIX guanine nucleotide exchange factor for Rac1 and Cdc42. J Biol Chem 278:19220-19229. CrossRef Medline
55. Poncer JC (2003) Hippocampal long term potentiation: silent synapses and beyond. J Physiol 97:415-422. CrossRef Medline
56. Poncer JC, Esteban JA, Malinow R (2002) Multiple mechanisms for the poentiation of AMPA receptor-mediated transmission by alpha-Ca 2 /calmodulin-dependent protein kinase II. J Neurosci 22:4406-4411. Medline
57. Puskarjov M, Ahmad F, Kaila K, Blaesse P (2012) Activity-dependent cleavage of the K-Cl cotransporter KCC2 mediated by calcium-activated protease calpain. J Neurosci 32:11356-11364. CrossRef Medline
58. Puskarjov M, Seja P, Heron SE, Williams TC, Ahmad F, Iona X, Oliver KL, Grinton BE, Vutskits L, Scheffer IE, Petrou S, Blaesse P, Dibbens LM, Berkovic SF, Kaila K (2014) A variant of KCC2 from patients with febrile seizures impairs neuronal Cl extrusion and dendritic spine formation. EMBO Rep 15:723-729. CrossRef Medline
59. Rho GJ, Kim DS, Son WJ, Cho SR, Kim JG, Choe SY (2007) Influence of in vitro oxygen concentrations on preimplantation embryo development, Chevy et al. KCC2 Gates LTP Expression at Hippocampal Synapses gene expression and production of Hanwoo calves following embryo transfer. Mol Reprod Dev 74:486-496. CrossRef Medline
60. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, Sixt M, Wedlich-Soldner R (2008) Life- Act: a versatile marker to visualize Factin. Nat Methods 5:605-607. CrossRef Medline
61. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K /Cl cotransporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255. CrossRef Medline
62. Rivera C, Voipio J, Thomas-Crusells J, Li H, Emri Z, Sipilä S, Payne JA, Minichiello L, Saarma M, Kaila K (2004) Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci 24:4683-4691. CrossRef Medline
63. Ross-Macdonald P, de Silva H, Guo Q, Xiao H, Hung CY, Penhallow B, Markwalder J, He L, Attar RM, Lin TA, Seitz S, Tilford C, Wardwell-Swanson J, Jackson D (2008) Identification of a nonkinase target mediating cytotoxicity of novel kinase inhibitors. Mol Cancer Ther 7:3490-3498. CrossRef Medline
64. Rust MB, Gurniak CB, Renner M, Vara H, Morando L, Görlich A, Sassoè- Pognetto M, Banchaabouchi MA, Giustetto M, Triller A, Choquet D, Witke W (2010) Learning, AMPA receptor mobility and synaptic plasticity depend on ncofilin-mediated actin dynamics. EMBO J 29:1889-1902. CrossRef Medline
65. Saneyoshi T, Wayman G, Fortin D, Davare M, Hoshi N, Nozaki N, Natsume T, Soderling TR (2008) Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 57:94-107. CrossRef Medline
66. Smith KR, Davenport EC, Wei J, Li X, Pathania M, Vaccaro V, Yan Z, Kittler JT (2014) GIT1 and betaPIX are essential for GABA(A) receptor synaptic stability and inhibitory neurotransmission. Cell Rep 9:298-310. CrossRef Medline
67. Tietz EI, Kapur J, Macdonald RL (1999) Functional GABAA receptor heterogeneity of acutely dissociated hippocampal CA1 pyramidal cells. J Neurophysiol 81:1575-1586. Medline
68. Tyzio R, Nardou R, Ferrari DC, Tsintsadze T, Shahrokhi A, Eftekhari S, Khalilov I, Tsintsadze V, Brouchoud C, Chazal G, Lemonnier E, Lozovaya N, Burnashev N, Ben-Ari Y (2014) Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 343:675-679. CrossRef Medline
69. Urban NT, Willig KI, Hell SW, Nägerl UV (2011) STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys J 101:1277-1284. CrossRef Medline
70. Wake H, Watanabe M, Moorhouse AJ, Kanematsu T, Horibe S, Matsukawa N, Asai K, Ojika K, Hirata M, Nabekura J (2007) Early changes in KCC2 phosphorylation in response to neuronal stress result in functional down- regulation. J Neurosci 27:1642-1650. CrossRef Medline
71. Watanabe M, Wake H, Moorhouse AJ, Nabekura J (2009) Clustering of neuronal K -Cl cotransporters in lipid rafts by tyrosine phosphorylation. J Biol Chem 284:27980-27988. CrossRef Medline
72. Woodin MA, Ganguly K, Poo MM (2003) Coincident pre-and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cltransporter activity. Neuron 39:807-820. CrossRef Medline
73. Zhang H, Webb DJ, Asmussen H, Horwitz AF (2003) Synapse formation is regulated by the signaling adaptor GIT1. J Cell Biol 161:131-142. CrossRef Medline