Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells

Journal of Neuroscience

Volumn 23, Issue 20, 2003, Pages 7489-7503

  Pereda, A ^a   O'Brien, J ^b   Nagy, J I ^c   Bukauskas, F ^a   Davidson, K G V ^d   Kamasawa, N ^d   Yasumura, T ^d   Rash, J E ^d  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF MANITOBA   (Canada)

^d Immunology and Pathology   (United States)

Author keywords

Auditory; Connexin36; Electrical coupling; Electrical synapse; Gap junction; NMDA; Synaptic plasticity

Indexed keywords

CONNEXIN 35; CONNEXIN 36; GAP JUNCTION PROTEIN; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL COMPOSITION; BRAIN; CELL MEMBRANE CONDUCTANCE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRIC CONDUCTIVITY; GAP JUNCTION; GOLDFISH; IMMUNOGOLD LABELING; MAMMAL; MAUTHNER CELL; NERVE CELL PLASTICITY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RHOMBENCEPHALON; SYNAPSE; SYNAPTIC TRANSMISSION; ULTRASTRUCTURE;

EID: 0042178306     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-20-07489.2003     Document Type: Article

References (60)

1. Al-Ubaidi MR, White TW, Ripps H, Poras I, Avner P, Gomes D, Bruzzone R (2000) Functional properties, developmental regulation, and chromosomal localization of murine connexin36, a gap-junctional protein expressed preferentially in retina and brain. J Neurosci Res 59:813-826.
2. Bartelmez GW (1915) Mauthner's cell and the nucleus motorius tegmenti. J Comp Neurol 25:87-128.
3. Belluardo N, Trovato-Salinaro A, Mudo G, Hurd YL, Condorelli DF (1999) Structure, chromosomal localization, and brain expression of human Cx36 gene. J Neurosci Res 57:740-752.
4. Bennett MVL (1977) Electrical transmission: a functional analysis and comparison with chemical transmission. In: Cellular biology of neurons, Vol I, Section I, Handbook of physiology. The nervous system (Kandel ER, ed), pp 357-416. Baltimore: Williams & Wilkins.
5. Bennett MVL, Aljure E, Nakajima Y, Pappas GD (1963) Electrotonic junctions between teleost spinal neurons: electrophysiology and ultrastructure. Science 141:262-264.
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.
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. Bukauskas FF, Jordan K, Bukauskiene A, Bennett MV, Lampe PD, Laird DW, Verselis VK (2000) Clustering of connexin 43-enhanced green fluorescent protein gap junction channels and functional coupling in living cells. Proc Natl Acad Sci USA 97:2556-2561.
9. 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.
10. Condorelli DF, Belluardo N, Trovato-Salinaro A, Mudo G (2000) Expression of Cx36 in mammalian neurons. Brain Res Rev 32:72-85.
11. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL (2001) Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31:477-485.
12. Dermietzel R, Spray DC (1993) Gap junctions in the brain: Where, what type, how many and why? Trends Neurosci 16:186-192.
13. Dermietzel R, Traub O, Hwang TK, Beyer E, Bennett MVL, Spray DC, Willecke K (1989) Differential expression of three gap junction proteins in developing and mature brain tissues. Proc Natl Acad Sci USA 86:10148-10152.
14. Dermietzel R, Hertzberg EL, Kessler JA, Spray DC (1991) Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis. J Neurosci 11:1421-1432.
15. Fujimoto K (1995) Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J Cell Sci 108:3443-3449.
16. Furshpan EJ (1964) Electrical transmission at an excitatory synapse in a vertebrate brain. Science 144:878-880.
17. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
18. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
19. Harris KM, Landis DMD (1986) Membrane structure at synaptic junctions in area CA1 of the rat hippocampus. Neuroscience 19:857-872.
20. Hormuzdi SG, Pais I, LeBeau FE, Towers SK, Rozov A, Buhl EH, Whittington MA, Monyer H (2001) Impaired electrical signaling disrupts gamma frequency oscillations in connexin36-deficient mice. Neuron 31:487-495.
21. Korn H, Sotelo C, Crepel F (1973) Electrotonic coupling between neurons in rat lateral vestibular nucleus. Exp Brain Res 16:255-275.
22. Korn H, Sotelo C, Bennett MVL (1977) The lateral vestibular nucleus of the toadfish Opsanus Tau: ultrastructural and electrophysiological observations with special reference to electrotonic transmission. Neuroscience 2:851-884.
23. Landisman CE, Long MA, Beierlein M, Deans MR, Paul DL, Connors BW (2002) Electrical synapses in the thalamic reticular nucleus. J Neurosci 22:1002-1009.
24. Lin JW, Faber DS (1988) 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.
25. Nagy JI, Dudek FE, Rash JE (2003) Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res Rev, in press.
26. Nakajima Y (1974) Fine structure of the synaptic endings on the Mauthner cell of the goldfish. J Comp Neurol 156:375-402.
27. O'Brien J, Al-Ubaidi MR, Ripps H (1996) Connexin35: a gap-junctional protein expressed preferentially in the skate retina. Mol Biol Cell 7:233-243.
28. 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.
29. Pereda A, Faber DS (1996) Activity dependent short-term plasticity of intercellular coupling. J Neurosci 16:983-992.
30. Pereda A, Bell T, Faber DS (1995) Retrograde synaptic communication via gap junctions coupling auditory afferents to the Mauthner cell. J Neurosci 15:5943-5955.
31. 2+/calmodulin-dependent kinase II mediates simultaneous enhancement of gap junctional conductance and glutamatergic transmission. Proc Natl Acad Sci USA 95:13272-13277.
32. Phillips TE, Boyne AF (1984) Liquid nitrogen-based quick freezing: experiments with bounce-free delivery of cholinergic nerve terminals to a metal surface. J Electron Microsc Tech 1:9-29.
33. Rash JE, Yasumura T (1999) Direct immunogold labeling of connexins and aquaporin4 in freeze-fracture replicas of liver, brain and spinal cord: factors limiting quantitative analysis. Cell Tissue Res 296:307-321.
34. Rash JE, Dillman RK, Bilhartz BL, Duffy HS, Whalen LR, Yasumura T (1996) Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc Natl Acad Sci USA 93:4235-4239.
35. Rash JE, Duffy HS, Dudek FE, Bilhartz BL, Whalen LR, Yasumura T (1997) Grid-mapped freeze-fracture analysis of gap junctions in gray and white matter of adult rat central nervous system, with evidence for a "panglial syncytium" that is not coupled to neurons. J Comp Neurol 388:265-292.
36. Rash JE, Yasumura T, Hudson CS, Agre P, Nielsen S (1998) Direct immunogold labeling of Aquaporin-4 in "square arrays" of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Pro Natl Acad Sci 95:11981-11986.
37. Rash JE, Yasumura T, Furman CS, Ottersen OP, Pereda AE, Dudek FE, Whalen LR, Staines WA, Nagy JI (2000) Excitatory mixed synapses in goldfish and rat: freeze-fracture replica immunogold labeling of glutamate receptor NR1 and connexin36. Soc Neurosci Abstr 26:1390.
38. Rash JE, Yasumura T, Dudek FE, Nagy JI (2001) Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J Neurosci 21:1983-2000.
39. Revel JP, Karnovsky MJ (1967) Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol 33:C7-C12.
40. Richter A, Precht W, Ozawa S (1975) Responses of neurons of lizard's, Lacerta viridis, vestibular nuclei to electrical stimulation of the ipsi- and contralateral VIIIth nerves. Pflügers Arch 355:85-94.
41. Robertson DJ, Bodenheomer TS, Stage D (1963) The ultrastructure of Mauthner cell synapses and nodes in goldfish brain. J Cell Biol 19:201-221.
42. Rovainen CM (1974) Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey. J Comp Neurol 154:207-223.
43. Severs NJ (1999) Cardiovascular disease. Novartis Found Symp 219:188-206.
44. Sloper JJ (1972) Gap junctions between dendrites in the primate cortex. Brain Res 44:641-646.
45. Smith M, Pereda A (2003) Chemical synaptic activity modulates nearby electrical synapses. Proc Natl Acad Sci USA 100:4849-4854.
46. Sohl G, Degen J, Teubner B, Willecke K (1998) The murine gap junction gene connexin36 is highly expressed in mouse retina and regulated during brain development. FEBS Lett 428:27-31.
47. 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.
48. Srinivas M, Rozental R, Kojima T, Dermietzel R, Mehler M, Condorelli DF, Kessler JA, Spray DC (1999) Functional properties of channels formed by the neuronal gap junction protein connexin36. J Neurosci 19:9848-9855.
49. Sur C, Wenthold R, Triller A (1994) Differential cellular distribution of excitatory amino acid receptor subunits on the M-cell of teleost. Soc Neurosci Abstr 20:489.
50. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618-624.
51. Teubner B, Degen J, Sohl G, Guldenagel M, Bukauskas FF, Trexler EB, Verselis VK, De Zeeuw CI, Lee CG, Kozak CA, Petrasch-Parwez E, Dermietzel R, Willecke K (2000) Functional expression of the murine connexin36 gene coding for a neuron-specific gap junctional protein. J Membr Biol 176:249-262.
52. 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.
53. Wolburg H, Kastner R, Kurz-Isler G (1983) Lack of orthogonal particle assemblies and presence of tight junctions in astrocytes of the goldfish (Carassius auratus). Cell Tissue Res 234:389-402.
54. Wolszon L, Pereda A, Faber DS (1997) A fast synaptic potential mediated by NMDA and non-NMDA receptors. J Neurophysiol 78:2693-2705.
55. Yang XD, Korn H, Faber DS (1990) Long-term potentiation of electrotonic coupling at mixed synapses. Nature 348:542-545.
56. Yox DP, Faber DS, Nicholson BJ (1990) Gap-junction antibody attenuates electrical coupling between the goldfish Mauthner (M-) cell and its eighth nerve afferents. Soc Neurosci Abstr 16:185.
57. Zottoli SJ, Danielson PD (1989) The lateral line afferent and efferent systems of the goldfish with special reference to the Mauthner cell. In: The mechanosensory lateral line: neurobiology and evolution (Coombs S, Görner P, Münz H, eds), pp 461-478. New York: Springer.
58. Zottoli SJ, Faber DS (1979) Properties and distribution of anterior VIIIth nerve excitatory inputs to the goldfish Mauthner cell. Brain Res 174:319-323.
59. Zottoli SJ, Van Horne C (1983) Posterior lateral line afferent and efferent pathways within the central nervous system of the goldfish with special reference to the Mauthner cell. J Comp Neurol 219:100-111.
60. Zottoli SJ, Bentley AP, Prendergast BJ, Rieff HI (1995) Comparative studies on the Mauthner cell of teleost fish in relation to sensory input. Brain Behav Evol 46:151-164.