Variability of distribution of Ca2+/calmodulin-dependent kinase II at mixed synapses on the mauthner cell: Colocalization and association with connexin 35

Journal of Neuroscience

Volumn 30, Issue 28, 2010, Pages 9488-9499

  Flores, Carmen E ^a,c   Cachope, Roger ^a   Nannapaneni, Srikant ^a   Ene, Smaranda ^a   Nairn, Angus C ^b   Pereda, Alberto E ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CONNEXIN 35; GAP JUNCTION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; CHEMICAL ANALYSIS; ELECTRICAL SYNAPSE; ENZYME ACTIVATION; ENZYME LOCALIZATION; GAP JUNCTION; GOLDFISH; MAUTHNER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TELEOST;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CONNEXINS; ELECTRICAL SYNAPSES; ELECTROPHYSIOLOGY; FLUORESCENT DYES; GAP JUNCTIONS; GLUTAMIC ACID; GOLDFISH; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; NEURONAL PLASTICITY; NEURONS; PRESYNAPTIC TERMINALS; SYNAPTIC TRANSMISSION;

EID: 77954724789     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4466-09.2010     Document Type: Article

References (70)

1. Alev C, Urschel S, Sonntag S, Zoidl G, Fort AG, Höher T, Matsubara M, Willecke K, Spray DC, Dermietzel R (2008) The neuronal connexin36 interacts with and is phosphorylated by CaMKII in a way similar to CaMKII interaction with glutamate receptors. Proc Natl Acad Sci U S A 105:20964-20969.
2. 2+-calmodulin-dependent kinase II. J Neurosci 27:14007-14011.
3. Bartelmez GW (1915) Mauthner's cell and the nucleus motorius tegmenti. J Comp Neurol 25:87-128.
4. Bartelmez GW, Hoerr NL (1933) The vestibular club endings in Ameiurus. Further evidence on the morphology of the synapse. J Comp Neurol 67:401-428.
5. Bayer KU, De Koninck P, Leonard AS, Hell JW, Schulman H (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411:801-805. (Pubitemid 32588103)
6. Berman N, Dunn RJ, Maler L (2001) Function of NMDA receptors and persistent sodium channels in a feedback pathway of the electrosensory system. J Neurophysiol 86:1612-1621. (Pubitemid 32953212)
7. Bodian D (1937) The structure of the vertebrate synapse. A study of the axon endings on Mauthner's cell and neighboring centers in the goldfish. J Comp Neurol 1:117-160.
8. Burr GS, Mitchell CK, Keflemariam YJ, Heidelberger R, O'Brien J (2005) Calcium-dependent binding of calmodulin to neuronal gap junction proteins. Biochem Biophys Res Commun 335:1191-1198. (Pubitemid 41215544)
9. Cachope R, Mackie K, Triller A, O'Brien J, Pereda AE (2007) Potentiation of electrical and chemical synaptic transmission mediated by endocannabinoids. Neuron 56:1034-1047. (Pubitemid 350251118)
10. Ciolofan C, Li XB, Olson C, Kamasawa N, Gebhardt BR, Yasumura T, Morita M, Rash JE, Nagy JI (2006) Association of connexin36 and zonula occludens-1 with zonula occludens-2 and the transcription factor zonula occludens-1-associated nucleic acid-binding protein at neuronal gap junctions in rodent retina. Neuroscience 140:433-451.
11. Condorelli DF, Parenti R, Spinella F, Trovato Salinaro A, Belluardo N, Cardile V, Cicirata F (1998) Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur J Neurosci 10:1202-1208. (Pubitemid 28375646)
12. Condorelli DF, Belluardo N, Trovato-Salinaro A, Mudò G (2000) Expression of Cx36 in mammalian neurons. Brain Res Rev 32:72-85.
13. Curti S, Pereda AE (2004) Voltage-dependent enhancement of electrical coupling by a sub-threshold sodium current. J Neurosci 24:3999-4010. (Pubitemid 38544226)
14. Curti S, Gómez L, Budelli R, Pereda AE (2008) Subthreshold sodium current underlies essential functional specializations at primary auditory afferents. J Neurophysiol 99:1683-1699. (Pubitemid 351550065)
15. 2+/calmodulin- kinase II enhances channel conductance of α-amino-3-hydroxy-5-methyl- isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci U S A 96:3269-3274.
16. Dosemeci A, Tao-Cheng JH, Vinade L, Winters CA, Pozzo-Miller L, Reese TS (2001) Glutamate-induced transient modification of the postsynaptic density. Proc Natl Acad Sci U S A 98:10428-10432. (Pubitemid 32803036)
17. Fink CC, Meyer T (2002) Molecular mechanisms of CaMKII activation in neuronal plasticity. Curr Opin Neurobiol 12:293-299. (Pubitemid 34615755)
18. Flores CE, Li X, Bennett MV, Nagy JI, Pereda AE (2008) Interaction between connexin 35 and zonula occludens 1 and its potential role in regulation of electrical synapses. Proc Natl Acad Sci U S A 105:12545-12550.
19. Fukami Y, Furukawa T, Asada Y (1965) Excitability changes of the Mauthner cell during collateral inhibition. J Gen Physiol 48:581-600.
20. Furshpan EJ (1964) "Electrical transmission" at an excitatory synapse in a vertebrate brain. Science 144:878-880.
21. Gleason MR, Higashijima S, Dallman J, Liu K, Mandel G, Fetcho JR (2003) Translocation of CaM kinase II to synaptic sites in vivo. Nat Neurosci 6:217-218. (Pubitemid 36278277)
22. Hervé JC, Bourmeyster N, Sarrouilhe D (2004) Diversity in protein-protein interactions of connexins: emerging roles. Biochim Biophys Acta 1662:22-41.
23. 2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu Rev Biochem 71:473-510.
24. Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S (1999) Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147:1351-1363.
25. Kennedy MB (2000) Signal-processing machines at the postsynaptic density. Science 290:750-754.
26. Kim E, Sheng M (2004) PDZ domain proteins of synapses. Nat Rev Neurosci 5:771-781.
27. Kothmann WW, Li X, Burr GS, O'Brien J (2007) Connexin 35/36 is phosphorylated at regulatory sites in the retina. Vis Neurosci 24:363-375.
28. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458:299-304.
29. Li X, Olson C, Lu S, Kamasawa N, Yasumura T, Rash JE, Nagy JI (2004a) Neuronal connexin36 association with zonula occludens-1 protein (ZO-1) in mouse brain and interaction with the first PDZ domain of ZO-1. Eur J Neurosci 19:2132-2146.
30. Li X, Olson C, Lu S, Nagy JI (2004b) Association of connexin36 with zonula occludens-1 in HeLa cells, betaTC-3 cells, pancreas, and adrenal gland. Histochem Cell Biol 122:485-498.
31. Li X, Lu S, Nagy JI (2009) Direct association of connexin36 with zonula occludens-2 and zonula occludens-3. Neurochem Int 54:393-402.
32. Liao D, Scannevin RH, Huganir R (2001) Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors. J Neurosci 21:6008-6017.
33. Lin JW, Faber DS (1988a) Synaptic transmission mediated by single club endings on the goldfish Mauthner cell. I. Characteristics of electrotonic and chemical postsynaptic potentials. J Neurosci 8:1302-1312.
34. Lin JW, Faber DS (1988b) Synaptic transmission mediated by single club endings on the goldfish Mauthner cell. II. Plasticity of excitatory postsynaptic potentials. J Neurosci 8:1313-1325.
35. Lin Y, Skeberdis VA, Francesconi A, Bennett MV, Zukin RS (2004) Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J Neurosci 24:10138-10148.
36. Malinow R, Mainen ZF, Hayashi Y (2000) LTP mechanisms: from silence to four-lane traffic. Curr Opin Neurobiol 10:352-357.
37. Merrill MA, Chen Y, Strack S, Hell JW (2005) Activity-driven postsynaptic translocation of CaMKII. Trends Pharmacol Sci 26:645-653.
38. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396:433-439.
39. Mitropoulou G, Bruzzone R (2003) Modulation of perch connexin35 hemichannels by cyclic AMP requires a protein kinase A phosphorylation site. J Neurosci Res 72:147-157.
40. Mori H, Manabe T, Watanabe M, Satoh Y, Suzuki N, Toki S, Nakamura K, Yagi T, Kushiya E, Takahashi T, Inoue Y, Sakimura K, Mishina M (1998) Role of the carboxy-terminal region of the GluR epsilon2 subunit in synaptic localization of the NMDA receptor channel. Neuron 21:571-580.
41. O'Brien J, Bruzzone R, White TW, Al-Ubaidi MR, Ripps H (1998) Cloning and expression of two related connexins from the perch retina define a distinct subgroup of the connexin family. J Neurosci 18:7625-7637.
42. 2+/calmodulin- dependent protein kinase binds to actin filaments in a calmodulin-sensitive manner. FEBS Lett 208:423-426.
43. Ouyang X, Winbow VM, Patel LS, Burr GS, Mitchell CK, O'Brien J (2005) Protein kinase A mediates regulation of gap junctions containing connexin35 through a complex pathway. Brain Res Mol Brain Res 135:1-11.
44. Pereda A, O'Brien J, Nagy JI, Bukauskas F, Davidson KG, Kamasawa N, Yasumura T, Rash JE (2003) Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci 23:7489-7503. (Pubitemid 37034065)
45. Pereda AE, Faber DS (1996) Activity dependent short-term plasticity of intercellular coupling. J Neurosci 16:983-992.
46. Pereda AE, Nairn AC, Wolszon LR, Faber DS (1994) Postsynaptic modulation of synaptic efficacy at mixed synapses on the Mauthner cell. J Neurosci 14:3704-3712.
47. 2+/calmodulin-dependent kinase II mediates simultaneous enhancement of gap junctional conductance and glutamatergic transmission. Proc Natl Acad Sci U S A 95:13272-13277.
48. Pereda AE, Rash JE, Nagy JI, Bennett MV (2004) Dynamics of electrical transmission at club endings on the Mauthner cells. Brain Res Rev 47:227-244.
49. Robertson JD, Bodenheimer TS, Stage DE (1963) The ultrastructure of Mauthner cell synapses and nodes in goldfish brains. J Cell Biol 19:159-199.
50. Rose J, Jin SX, Craig AM (2009) Heterosynaptic molecular dynamics: locally induced propagating synaptic accumulation of CaM kinase II. Neuron 61:351-358.
51. Rosenberg OS, Deindl S, Sung RJ, Nairn AC, Kuriyan J (2005) Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme. Cell 123:849-860. (Pubitemid 41721031)
52. Sahyoun N, LeVine H 3rd, Bronson D, Siegel-Greenstein F, Cuatrecasas P (1985) Cytoskeletal calmodulin-dependent protein kinase. Characterization, solubilization, and purification from rat brain. J Biol Chem 260:1230-1237. (Pubitemid 15173642)
53. Schulman H (2004) Activity-dependent regulation of calcium/calmodulin- dependent protein kinase II localization. J Neurosci 24:8399-8403. (Pubitemid 39313760)
54. Shen K, Meyer T (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284:162-166. (Pubitemid 29282073)
55. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343. (Pubitemid 32455340)
56. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-1816.
57. Singla SI, Hudmon A, Goldberg JM, Smith JL, Schulman H(2001) Molecular characterization of calmodulin trapping by calcium/calmodulin-dependent protein kinase II. J Biol Chem 276:29353-29360.
58. Smith M, Pereda AE (2003) Chemical synaptic activity modulates nearby electrical synapses. Proc Natl Acad Sci U S A 100:4849-4854.
59. Sotelo C, Korn H (1978) Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. Int Rev Cytol 55:67-107.
60. Sprengel R, Suchanek B, Amico C, Brusa R, Burnashev N, Rozov A, Hvalby O, Jensen V, Paulsen O, Andersen P, Kim JJ, Thompson RF, Sun W, Webster LC, Grant SG, Eilers J, Konnerth A, Li J, McNamara JO, Seeburg PH (1998) Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 92:279-289.
61. Steigerwald F, Schulz TW, Schenker LT, Kennedy MB, Seeburg PH, Köhr G (2000) C-Terminal truncation of NR2A subunits impairs synaptic but not extrasynaptic localization of NMDA receptors. J Neurosci 20:4573-4581.
62. Strack S, McNeill RB, Colbran RJ (2000) Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B sub-unit of the N-methyl-D-aspartate receptor. J Biol Chem 275:23798-23806.
63. Sun XX, Hodge JJ, Zhou Y, Nguyen M, Griffith LC (2004) The eag potassium channel binds and locally activates calcium/calmodulin-dependent protein kinase II. J Biol Chem 279:10206-10214.
64. Tuttle R, Masuko S, Nakajima Y (1986) Freeze fracture study of the large myelinated club ending synapse on the goldfish Mauthner cell: special reference to the quantitative analysis of gap junctions. J Comp Neurol 246:202-211.
65. Urschel S, Höher T, Schubert T, Alev C, Söhl G, Wörsdörfer P, Asahara T, Dermietzel R, Weiler R, Willecke K (2006) Protein kinase A-mediated phosphorylation of connexin36 in mouse retina results in decreased gap junctional communication between AII amacrine cells. J Biol Chem 281:33163-33171.
66. Wayman GA, Lee YS, Tokumitsu H, Silva AJ, Soderling TR (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59:914-931.
67. Wolszon LR, Pereda AE, Faber DS (1997) A fast synaptic potential mediated by NMDA and non-NMDA receptors. J Neurophysiol 78:2693-2706.
68. Xue Y, Ren J, Gao X, Jin C, Wen L, Yao X (2008) GPS 2.0, a tool to predict kinase-specific phosphorylation sites in hierarchy. Mol Cell Proteomics 7:1598-1608.
69. Yang E, Schulman H (1999) Structural examination of autoregulation of multifunctional calcium/calmodulin-dependent protein kinase II. J Biol Chem 274:26199-26208.
70. Yang XD, Korn H, Faber DS (1990) Long-term potentiation of electrotonic coupling at mixed synapses. Nature 348:542-545.