Connexin36 vs. connexin32, "miniature" neuronal gap junctions, and limited electrotonic coupling in rodent suprachiasmatic nucleus

Neuroscience

Volumn 149, Issue 2, 2007, Pages 350-371

  Rash, J E ^a   Olson, C O ^b   Pouliot, W A ^a,c   Davidson, K G V ^a   Yasumura, T ^a   Furman, C S ^a,d   Royer, S ^a   Kamasawa, N ^a   Nagy, J I ^b   Dudek, F E ^a,c  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

electrical synapse; freeze fracture replica immunogold labeling; immunocytochemistry; metabolic coupling; spikelet; synchrony

Indexed keywords

CONNEXIN 30; CONNEXIN 32; CONNEXIN 36; CONNEXIN 43; LIDOCAINE ETHOBROMIDE;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; CELL POPULATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; ELECTRON MICROSCOPY; FEMALE; FREEZE FRACTURE; GAP JUNCTION; HYPOTHALAMUS; IMMUNOFLUORESCENCE MICROSCOPY; MALE; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SUPRACHIASMATIC NUCLEUS; ULTRASTRUCTURE;

ANIMALS; CONNEXINS; DETERGENTS; ELECTROPHYSIOLOGY; FREEZE FRACTURING; GAP JUNCTIONS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NEUROGLIA; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SODIUM DODECYL SULFATE; SUPRACHIASMATIC NUCLEUS;

EID: 35348907863     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.06.052     Document Type: Article

References (87)

1. Balice-Gordon R.J., Bone L.J., and Scherer S.S. Functional gap junctions in the Schwann cell myelin sheath. J Cell Biol 142 (1998) 1095-1104
2. Bennett M.V.L., and Zukin R.S. Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41 (2004) 495-511
3. Berdan R.C., Shivers R.R., and Bulloch A.G.M. Chemical synapses, particle arrays, pseudo-gap junctions and gap junctions of neurons and glia in the buccal ganglion of Helisoma. Synapse 1 (1987) 304-323
4. Bouskila Y., and Dudek F.E. Neuronal synchronization without calcium-dependent synaptic transmission in the hypothalamus. Proc Natl Acad Sci U S A 90 (1993) 3207-3210
5. Branton D., Bullivant S., Gilula N.B., Karnovsky M.J., Moor H., Northcote D.H., Packer L., Satir B., Satir P., Speth V., Staehelin L.A., Steere R.L., and Weinstein R.S. Freeze-etching nomenclature. Science 190 (1975) 54-56
6. Brightman M.W., and Reese T.S. Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40 (1969) 648-677
7. Bushong E.A., Martone M.E., Jones Y.Z., and Ellisman M.H. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22 (2002) 183-192
8. Castel M., Belenky M., Cohen S., Ottersen O.P., and Storm-Mathisen J. Glutamate-like immunoreactivity in retinal terminals of the mouse suprachiasmatic nucleus. Eur J Neurosci 5 (1993) 368-381
9. Challcroft J.P., and Bullivant S. An interpretation of liver cell membrane and junction structure based on observation of freeze-fracture replicas of both sides of the fracture. J Cell Biol 47 (1970) 49-60
10. Colwell C. Rhythmic coupling among cells in the suprachiasmatic nucleus. J Neurobiol 43 (2000) 379-388
11. Condorelli D.F., Parenti R., Spinella F., Salinaro A.T., Belluardo N., Cardile V., and Cicirata F. Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur J Neurosci 10 (1998) 1202-1208
12. Deans M.R., Gibson J.R., Sellitto C., Connors B.W., and Paul D.L. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31 (2001) 477-485
13. Dudek F.E., Andrew R.D., MacVicar B.A., Snow R.W., and Taylor C.P. Recent evidence for and possible significance of gap junctions in electrotonic synapses in mammalian brain. In: Jasper H.H., and van Gelder N.M. (Eds). Basic mechanisms of neuronal hyperexcitability (1983), Alan R. Liss, New York 31-73
14. Eyzaguirre C., and Kuffler S.W. Processes of excitation in the dendrites and in the soma of single isolated sensory nerve cells of the lobster and crayfish. J Gen Physiol 39 (1955) 87-119
15. Fujimoto K. 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 (1995) 3443-3449
16. Fujimoto K. SDS-digested freeze-fracture replica labeling electron microscopy to study the two-dimensional distribution of integral membrane proteins and phospholipids in biomembranes: practical procedure, interpretation and application. Histochem Cell Biol 107 (1997) 87-96
17. Fukuda T., Kosaka T., Singer W., and Galuske R.A.W. Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network. J Neurosci 26 (2006) 3434-3443
18. Fulton B.P., Miledi R., and Takahashi T. Electrical synapses between motoneurons in the spinal cord of the newborn rat. Proc R Soc Lond B 206 (1980) 115-120
19. Furman C.S., Gorelick-Feldman D.A., Davidson K.G.V., Yasumura T., Neely J.D., Agre P., and Rash J.E. Aquaporin-4 square array assembly: Opposing actions of M1 and M23 isoforms. Proc Natl Acad Sci U S A 100 (2003) 13609-13614
20. Gilula N.B., Reeves O.R., and Steinbach A. Metabolic coupling, ionic coupling and cell contacts. Nature 235 (1972) 262-265
21. Green D.J., and Gillette R. Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res 245 (1982) 198-200
22. Gribkoff V.K., Pieschl R.L., and Dudek F.E. GABA receptor-mediated inhibition of neuronal activity in rat SCN in vitro: pharmacology and influence of circadian phase. J Neurophysiol 90 (2003) 1438-1448
23. Gruijters W.T., Kistler J., Bullivant S., and Goodenough D.A. Immunolocalization of MP70 in lens fiber 16-17-nm intercellular junctions. J Cell Biol 104 (1987) 565-572
24. Hastings M.H., and Herzog E.D. Clock genes, oscillators, and cellular networks in the suprachiasmatic nuclei. J Biol Rhythms 19 (2004) 400-413
25. Herzog E.D., Grace M.S., Harrer C., Williamson J., Shinohara K., and Block G.D. The role of clock in the developmental expression of neuropeptides in the suprachiasmatic nucleus. J Comp Neurol 424 (2000) 86-98
26. Hombach S., Janssen-Bienhold U., Söhl G., Schubert T., Bussow H., Ott T., Weiler R., and Willecke K. Functional expression of connexin57 in horizontal cells of the mouse retina. Eur J Neurosci 19 (2004) 2633-2640
27. Honma S., Nakamura W., Shirakawa T., and Honma K.I. Diversity in the circadian periods of single neurons of the rat suprachiasmatic nucleus depends on nuclear structure and intrinsic period. Neurosci Lett 358 (2004) 173-176
28. Honma S., Shirakawa T., Katsuno Y., Namihira M., and Honma K.I. Circadian periods of single suprachiasmatic neurons in rats. Neurosci Lett 250 (1998) 157-160
29. Ibata Y., Okamura H., Tanaka M., Tamada Y., Hayashi S., Iijima N., Matsuda T.O., Munekawa K., Takamatsu T., and Hisa Y. Functional morphology of the suprachiasmatic nucleus. Front Neuroendocrinol 20 (1999) 241-268
30. Jiang Z.G., Yang Y.Q., and Allen C.N. Tracer and electrical coupling of rat suprachiasmatic nucleus. Neuroscience 77 (1997) 1059-1066
31. Jobst E.E., Robinson D.W., and Allen C.N. Potential pathways for intercellular communication within the calbindin subnucleus of the hamster suprachiasmatic nucleus. Neuroscience 123 (2004) 87-99
32. Kamasawa N., Furman C.S., Davidson K.G.V., Sampson J.A., Magnie A.R., Gebhardt B., Kamasawa M., Morita M., Yasumura T., Pieper M., Zumbrunnen J.R., Pickard G.E., Nagy J.I., and Rash J.E. Abundance and ultrastructural diversity of neuronal gap junctions in the OFF and ON sublaminae of the inner plexiform layer of rat and mouse retina. Neuroscience 142 (2006) 1093-1117
33. Kamasawa N., Sik A., Morita M., Yasumura T., Davidson K.G.V., Nagy J.I., and Rash J.E. Connexin47 and connexin32 in gap junctions of oligodendrocyte somata, myelin sheaths, paranodal loops, and Schmidt-Lanterman incisures: Implications for ionic homeostasis and potassium siphoning. Neuroscience 136 (2005) 65-86
34. Kim Y.I., and Dudek F.E. Intracellular electrophysiological study of suprachiasmatic neurons in rodents: excitatory synaptic mechanisms. J Physiol 444 (1991) 269-287
35. Kim Y.I., and Dudek F.E. Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: inhibitory synaptic mechanisms. J Physiol 458 (1992) 247-260
36. Kita H., and Armstrong W. A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: Comparison with biocytin. J Neurosci Methods 37 (1991) 141-150
37. Landis D.M.D., and Reese T.S. Arrays of particles in freeze-fractured astrocytic membranes. J Cell Biol 60 (1974) 316-320
38. Li J., Hertzberg E.L., and Nagy J.I. Connexin32 in oligodendrocytes and association with myelinated fibers in mouse and rat brain. J Comp Neurol 379 (1997) 571-591
39. Li X., Olson C., Lu S., Kamasawa N., Yasumura T., Rash J.E., and Nagy J.I. 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 (2004) 2132-2146
40. Liu C., and Reppert S.M. GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 25 (2000) 123-128
41. Long M.A., Jutras M.J., Connors B.W., and Burwell R.D. Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat Neurosci 8 (2005) 61-66
42. MacVicar B.A., and Dudek F.E. Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213 (1981) 782-785
43. Massa P.T., and Mugnaini E. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study. Neuroscience 7 (1982) 523-538
44. Massey S.C., O'Brien J.J., Trexler E.B., Li W., Keung J.W., Mills S.L., and O'Brien J. Multiple neuronal connexins in the mammalian retina. Cell Commun Adhes 10 (2003) 425-430
45. Matsumoto A., Arnold A.P., and Micevych P.E. Gap junctions between lateral spinal motoneurons in the rat. Brain Res 495 (1989) 362-366
46. Matsumoto A., Arnold A.P., Zampighi G., and Micevych P.E. Androgenic regulation of gap junctions between motoneurons in the rat spinal cord. J Neurosci 8 11 (1988) 4177-4183
47. Meier C., Dermietzel R., Davidson K.G.V., Yasumura T., and Rash J.E. Connexin32-containing gap junctions in Schwann cells at the internodal zone of partial myelin compaction and in Schmidt-Lanterman incisures. J Neurosci 24 (2004) 3186-3198
48. Mintz E.M., Marvel C.L., Gillespie C.F., Price K.M., and Albers H.E. Activation of NMDA receptors in the suprachiasmatic nucleus produces light-like phase shifts of the circadian clock in vivo. J Neurosci 19 (1999) 5124-5130
49. Mugnaini E. Cell junctions of astrocytes, ependyma, and related cells in the mammalian central nervous system, with emphasis on the hypothesis of a generalized functional syncytium of supporting cells. In: Fedoroff S., and Vernadakis A. (Eds). Astrocytes Vol. I (1986), Academic Press, New York 329-371
50. Nagy J.I., Dudek F.E., and Rash J.E. Update on connexins and gap junctions in neurons and glia in the mammalian central nervous system. Brain Res Brain Res Rev 47 (2004) 191-215
51. Nagy J.I., Ionescu A.-V., Lynn B.D., and Rash J.E. Connexin29 and connexin32 at oligodendrocyte and astrocyte gap junctions and in myelin of the mouse central nervous system. J Comp Neurol 464 (2003) 356-370
52. Nagy J.I., Ionescu A.-V., Lynn B.D., and Rash J.E. Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: Implications from normal and connexin32 knockout mice. Glia 44 (2003) 205-218
53. O'Brien J.J., Li W., Pan F., Keung J., O'Brien J., and Massey S.C. Coupling between A-type horizontal cells is mediated by connexin 50 gap junctions in the rabbit retina. J Neurosci 26 (2006) 11624-11636
54. Phillips T.E., and Boyne A.F. Liquid nitrogen-based quick freezing: Experiments with bounce-free delivery of cholinergic nerve terminals to a metal surface. J Electron Microsc Tech 1 (1984) 9-29
55. Rash J.E., Davidson K.G.V., Kamasawa N., Yasumura T., Kamasawa M., Zhang C., Michaels R., Restrepo D., Ottersen O.P., Olson C., and Nagy J.I. Ultrastructural localization of connexins (Cx36, Cx43, Cx45), glutamate receptors and aquaporin-4 in rodent olfactory mucosa, olfactory nerve and olfactory bulb. J Neurocytol 34 (2005) 307-341
56. Rash J.E., Davidson K.G.V., Yasumura T., and Furman C.S. Freeze-fracture and immunogold analysis of aquaporin-4 (AQP4) square arrays, with models of AQP4 lattice assembly. Neuroscience 129 (2004) 915-934
57. Rash J.E., Pereda A., Kamasawa N., Furman C.S., Yasumura T., Davidson K.G.V., Dudek F.E., Olson C., and Nagy J.I. High-resolution proteomic mapping in the vertebrate central nervous system: Close proximity of connexin35 to NMDA glutamate receptor clusters and co-localization of connexin36 with immunoreactivity for zonula occludens protein-1 (ZO-1). J Neurocytol 33 (2004) 131-152
58. Rash J.E., Dillman R.K., Bilhartz B.L., Duffy H.S., Whalen L.R., and Yasumura T. Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc Natl Acad Sci U S A 93 (1996) 4235-4239
59. Rash J.E., Dillman R.K., Morita M., Whalen L.R., Guthrie P.B., Fay-Guthrie D., and Wheeler D.W. Grid-mapped freeze fracture: Correlative confocal laser scanning microscopy and freeze-fracture electron microscopy of preselected cells in tissue slices. In: Severs N.J., and Shotton D.M. (Eds). Rapid freezing, freeze fracture, and deep etching (1995), Wiley-Liss, Inc, New York 127-150
60. Rash J.E., Duffy H.S., Dudek F.E., Bilhartz B.L., Whalen L.R., and Yasumura T. 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 (1997) 265-292
61. Rash J.E., Johnson T.J.A., Dinchuk J.E., Duch D.S., and Levinson S.R. Labeling intramembrane particles in freeze-fracture replicas. In: Hui S.W. (Ed). Freeze-fracture studies of membranes (1989), CRC Press, Boca Raton 41-59
62. Rash J.E., Olson C., Davidson K.G.V., Yasumura T., Kamasawa N., and Nagy J.I. Identification of connexin36 in gap junctions between neurons in rodent locus coeruleus. Neuroscience 147 (2007) 938-956
63. Rash J.E., Staines W.A., Yasumura T., Patel D., Hudson C.S., Stelmack G.L., and Nagy J.I. Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin36 (Cx36) but not Cx32 or Cx43. Proc Natl Acad Sci U S A 97 (2000) 7573-7578
64. Rash J.E., and Yasumura T. 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 (1999) 307-321
65. Rash J.E., Yasumura T., Davidson K., Furman C.S., Dudek F.E., and Nagy J.I. Identification of cells expressing Cx43, Cx30, Cx26, Cx32 and Cx36 in gap junctions of rat brain and spinal cord. Cell Commun Adhes 8 (2001) 315-320
66. Rash J.E., Yasumura T., Dudek F.E., and Nagy J.I. Cell-specific expression of connexins, and evidence for restricted gap junctional coupling between glial cells and between neurons. J Neurosci 21 (2001) 1983-2001
67. Rash J.E., Yasumura T., and Dudek F.E. Ultrastructure, histological distribution, and freeze-fracture immunocytochemistry of gap junctions in rat brain and spinal cord. Cell Biol Int 22 (1998) 731-749
68. Rash J.E., Yasumura T., Hudson C.S., Agre P., and Nielsen S. Direct immunogold labeling of aquaporin-4 in "square arrays" of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc Natl Acad Sci U S A 95 (1998) 11981-11986
69. Raviola E., and Gilula N.B. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. J Cell Biol 65 (1975) 192-222
70. Raviola E., Goodenough D.A., and Raviola G. Structure of rapidly frozen gap junctions. J Cell Biol 87 (1980) 273-279
71. Saper C.B., Lu J., Chou T.C., and Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci 28 (2005) 152-157
72. Schwartz W.J., Gross R.A., and Morton M.T. The suprachiasmatic nuclei contain a tetrodotoxin-resistant circadian pacemaker. Proc Natl Acad Sci U S A 84 (1987) 1694-1698
73. Sloper J.J. Gap junctions between dendrites in the primate cortex. Brain Res 44 (1972) 641-646
74. Söhl G., and Willecke K. An update on connexin genes and their nomenclature in mouse and man. Cell Commun Adhes 10 (2003) 173-180
75. Sotelo C., and Korn H. Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. Int Rev Cytol 55 (1978) 67-107
76. Spencer W.A., and Kandel E.R. Electrophysiology of hippocampal neurons: IV. Fast prepotentials. J Neurophysiol 24 (1961) 272-285
77. Steere R.L., and Moseley M. New dimensions in freeze-etching. Proc Elec Microsc Soc Am 27 (1969) 202-203
78. Strecker G.J., Wuarin J.P., and Dudek F.E. GABAA-mediated local synaptic pathways connect neurons in the rat suprachiasmatic nucleus. J Neurophysiol 78 (1997) 2217-2220
79. Stuart G.J., and Sakmann B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367 (1994) 69-72
80. van den Pol A.N. The hypothalamic suprachiasmatic nucleus of the rat: intrinsic anatomy. J Comp Neurol 91 (1980) 661-702
81. van den Pol A.N., and Dudek F.E. Cellular communication in the circadian clock, the suprachiasmatic nucleus. Neuroscience 56 (1993) 793-811
82. Wagner S., Castel M., Gainer H., and Yarom Y. GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 387 (2006) 598-603
83. Walton K.D., and Navarette R. Postnatal changes in motoneurone electronic coupling studied in the in vitro rat lumbar spinal cord. J Physiol (Lond) 433 (1991) 283-305
84. Welsh D.K., Logothetis D.E., Meister M., and Reppert S.M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14 (1995) 697-706
85. Welsh D.K., and Reppert S.M. Gap junctions couple astrocytes but not neurons in dissociated cultures of rat suprachiasmatic nucleus. Brain Res 706 (1996) 30-36
86. Wheal H.V., and Thomson A.M. The electrical properties of neurones of the rat suprachiasmatic nucleus recorded intracellularly in vitro. Neuroscience 13 (1984) 97-104
87. Willecke K., Eiberger J., Degen J., Eckardt D., Romualdi A., Gueldenagel M., Deutsch U., and Soehl G. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem 383 (2002) 725-737