Coupling between A-Type horizontal cells is mediated by connexin 50 gap junctions in the rabbit retina

Journal of Neuroscience

Volumn 26, Issue 45, 2006, Pages 11624-11636

  O'Brien, Jennifer J ^a   Li, Wei ^a,b   Pan, Feng ^a   Keung, Joyce ^a   O'Brien, John ^a   Massey, Stephen C ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Confocal microscopy; Connexin 50; Dye coupling; Gap junctions; Horizontal cells; Retina

Indexed keywords

CALBINDIN; COMPLEMENTARY DNA; DYE; GAP JUNCTION PROTEIN; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELL SIZE; CELL TYPE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC CELL; EXTRACELLULAR MATRIX; GENETIC CODE; GENETIC LINKAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RABBIT; RETINA; RETINA CONE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING;

ANIMALS; BASE SEQUENCE; BIOTIN; BLOTTING, NORTHERN; BLOTTING, WESTERN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CONNEXINS; DENDRITES; EYE PROTEINS; GAP JUNCTIONS; GENE EXPRESSION; ISOQUINOLINES; RABBITS; RETINA; RETINAL HORIZONTAL CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 33751110626     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2296-06.2006     Document Type: Article

References (65)

1. Ames III A, Nesbett FB (1981) In vitro retina as an experimental model of the central nervous system. J Neurochem 37:867-877.
2. Beyer EC, Reed KE, Westphale EM, Kanter HL, Larson DM (1992) Molecular cloning and expression of rat connexin40, a gap junction protein expressed in vascular smooth muscle. J Membr Biol 127:69-76.
3. Bloomfield SA, Miller RF (1982) A physiological and morphological study of the horizontal cell types of the rabbit retina. J Comp Neurol 208:288-303.
4. Bloomfield SA, Xin D, Persky SE (1995) A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina. Vis Neurosci 12:985-999.
5. Boycott BB, Peichl L, Wässle H (1978) Morphological types of horizontal cell in the retina of the domestic cat. Proc R Soc Lond B Biol Sci 203:229-245.
6. 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.
7. Caspar DL, Goodenough DA, Makowski L, Phillips WC (1977) Gap junction structures. I. Correlated electron microscopy and x-ray diffraction. J Cell Biol 74:605-628.
8. Chandross KJ, Spray DC, Cohen RI, Kumar NM, Kremer M, Dermietzel R, Kessler JA (1996) TNF alpha inhibits Schwann cell proliferation, connexin46 expression, and gap junctional communication. Mol Cell Neurosci 7:479-500.
9. Dacheux RF, Raviola E (1982) Horizontal cells in the retina of the rabbit. J Neurosci 2:1486-1493.
10. Deans MR, Paul DL (2001) Mouse horizontal cells do not express connexin26 or connexin36. Cell Adhes Commun 8:361-366.
11. Deans MR, Volgyi B, Goodenough DA, Bloomfield SA, Paul DL (2002) Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36:703-712.
12. DeVries SH (2000) Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28:847-856.
13. DeVries SH, Schwartz EA (1989) Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. J Physiol (Lond) 414:351-375.
14. DeVries SH, Schwartz EA (1992) Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. J Physiol (Lond) 445:201-230.
15. Dmitriev AV, Mangel SC (2001) Circadian clock regulation of pH in the rabbit retina. J Neurosci 21:2897-2902.
16. Feigenspan A, Teubner B, Willecke K, Weiler R (2001) Expression of neuronal connexin36 in AII amacrine cells of the mammalian retina. J Neurosci 21:230-239.
17. Feigenspan A, Janssen-Bienhold U, Hormuzdi S, Monyer H, Degen J, Sohl G, Willecke K, Ammermuller J, Weiler R (2004) Expression of connexin36 in cone pedicles and OFF-cone bipolar cells of the mouse retina. J Neurosci 24:3325-3334.
18. Goodenough DA, Paul DL (2003) Beyond the gap: functions of unpaired connexon channels. Nat Rev Mol Cell Biol 4:285-294.
19. Gros D, Jarry-Guichard T, Ten Velde I, de Maziere A, van Kempen MJ, Davoust J, Briand JP, Moorman AF, Jongsma HJ (1994) Restricted distribution of connexin40, a gap junctional protein, in mammalian heart. Circ Res 74:839-851.
20. Guldenagel M, Sohl G, Plum A, Traub O, Teubner B, Weiler R, Willecke K (2000) Expression patterns of connexin genes in mouse retina. J Comp Neurol 425:193-201.
21. Hampson EC, Weiler R, Vaney DI (1994) pH-gated dopaminergic modulation of horizontal cell gap junctions in mammalian retina. Proc R Soc Lond B Biol Sci 255:67-72.
22. Haverkamp S, Grunert U, Wassle H (2000) The cone pedicle, a complex synapse in the retina. Neuron 27:85-95.
23. Haverkamp S, Grunert U, Wässle H (2001) Localization of kainate receptors at the cone pedicles of the primate retina. J Comp Neurol 436:471-486.
24. Haverkamp S, Ghosh KK, Hirano AA, Wässle H (2003) Immunocytochemical description of five bipolar cell types of the mouse retina. J Comp Neurol 455:463-476.
25. He S, Weiler R, Vaney DI (2000) Endogenous dopaminergic regulation of horizontal cell coupling in the mammalian retina. J Comp Neurol 418:33-40.
26. Hennemann H, Suchyna T, Lichtenberg-Frate H, Jungbluth S, Dahl E, Schwarz J, Nicholson BJ, Willecke K (1992) Molecular cloning and functional expression of mouse connexin40, a second gap junction gene preferentially expressed in lung. J Cell Biol 117:1299-1310.
27. Hombach S, Janssen-Bienhold U, Sohl G, Schubert T, Bussow H, Ott T, Weiler R, Willecke K (2004) Functional expression of connexin57 in horizontal cells of the mouse retina. Eur J Neurosci 19:2633-2640.
28. Huang H, Li H, He SG (2005) Identification of connexin 50 and 57 mRNA in A-type horizontal cells of the rabbit retina. Cell Res 15:207-211.
29. Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R (2001) Hemichannel-mediated inhibition in the outer retina. Science 292:1178-1180.
30. Kanter HL, Saffitz JE, Beyer EC (1994) Molecular cloning of two human cardiac gap junction proteins, connexin40 and connexin45. J Mol Cell Cardiol 26:861-868.
31. Kolb H (1977) The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations. J Neurocytol 6:131-153.
32. Lauf U, Giepmans BN, Lopez P, Braconnot S, Chen SC, Falk MM (2002) Dynamic trafficking and delivery of connexons to the plasma membrane and accretion to gap junctions in living cells. Proc Natl Acad Sci USA 99:10446-10451.
33. Lee EJ, Han JW, Kim HJ, Kim IB, Lee MY, Oh SJ, Chung JW, Chun MH (2003) The immunocytochemical localization of connexin 36 at rod and cone gap junctions in the guinea pig retina. Eur J Neurosci 18:2925-2934.
34. Li W, DeVries SH (2004) Separate blue and green cone networks in the mammalian retina. Nat Neurosci 7:751-756.
35. Li W, Trexler EB, Massey SC (2002) Glutamate receptors at rod bipolar ribbon synapses in the rabbit retina. J Comp Neurol 448:230-248.
36. Lin JS, Fitzgerald S, Dong Y, Knight C, Donaldson P, Kistler J (1997) Processing of the gap junction protein connexin50 in the ocular lens is accomplished by calpain. Eur J Cell Biol 73:141-149.
37. Lin JS, Eckert R, Kistler J, Donaldson P (1998) Spatial differences in gap junction gating in the lens are a consequence of connexin cleavage. Eur J Cell Biol 76:246-250.
38. Massey SC, Mills SL (1996) A calbindin-immunoreactive cone bipolar cell type in the rabbit retina. J Comp Neurol 366:15-33.
39. Matesic D, Tillen T, Sitaramayya A (2003) Connexin 40 expression in bovine and rat retinas. Cell Biol Int 27:89-99.
40. Maxeiner S, Dedek K, Janssen-Bienhold U, Ammermuller J, Brune H, Kirsch T, Pieper M, Degen J, Kruger O, Willecke K, Weiler R (2005) Deletion of connexin45 in mouse retinal neurons disrupts the rod/cone signaling pathway between AII amacrine and ON cone bipolar cells and leads to impaired visual transmission. J Neurosci 25:566-576.
41. Mills SL, Massey SC (1991) Labeling and distribution of AII amacrine cells in the rabbit retina. J Comp Neurol 304:491-501.
42. Mills SL, Massey SC (1994) Distribution and coverage of A- and B-type horizontal cells stained with Neurobiotin in the rabbit retina. Vis Neurosci 11:549-560.
43. Mills SL, Massey SC (1998) The kinetics of tracer movement through homologous gap junctions in the rabbit retina. Vis Neurosci 15:765-777.
44. Mills SL, Massey SC (2000) A series of biotinylated tracers distinguishes three types of gap junction in retina. J Neurosci 20:8629-8636.
45. Mills SL, O'Brien JJ, Li W, O'Brien J, Massey SC (2001) Rod pathways in the mammalian retina use connexin36. J Comp Neurol 436:336-350.
46. Nelson R, von Litzow A, Kolb H, Gouras P (1975) Horizontal cells in cat retina with independent dendritic systems. Science 189:137-139.
47. Peichl L, Gonzalez-Soriano J (1994) Morphological types of horizontal cell in rodent retinae: a comparison of rat, mouse, gerbil, and guinea pig. Vis Neurosci 11:501-517.
48. Peracchia C (1977) Gap junctions. Structural changes after uncoupling procedures. J Cell Biol 72:628-641.
49. Raviola E, Dacheux RF (1990) Axonless horizontal cells of the rabbit retina: synaptic connections and origin of the rod aftereffect. J Neurocytol 19:731-736.
50. Raviola E, Gilula NB (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol 65:192-222.
51. Rohrenbeck J, Wassle H, Heizmann CW (1987) Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Neurosci Lett 77:255-260.
52. Schubert T, Maxeiner S, Kruger O, Willecke K, Weiler R (2005) Connexin45 mediates gap junctional coupling of bistratified ganglion cells in the mouse retina. J Comp Neurol 490:29-39.
53. 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.
54. Srinivas M, Costa M, Gao Y, Fort A, Fishman GI, Spray DC (1999) Voltage dependence of macroscopic and unitary currents of gap junction channels formed by mouse connexin50 expressed in rat neuroblastoma cells. J Physiol (Lond) 517:673-689.
55. Tenorio F, Giraldi-Guimaraes A, Mendez-Otero R (1996) Morphology of NADPH-diaphorase-positive cells in the retinoceptive layers of the developing rat superior colliculus. Int J Dev Neurosci 14:1-10.
56. Teranishi T, Negishi K, Kato S (1984) Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. J Neurosci 4:1271-1280.
57. Vaney DI (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci Lett 125:187-190.
58. Vaney DI (1993) The coupling pattern of axon-bearing horizontal cells in the mammalian retina. Proc R Soc Lond B Biol Sci 252:93-101.
59. Volgyi B, Abrams J, Paul DL, Bloomfield SA (2005) Morphology and tracer coupling pattern of alpha ganglion cells in the mouse retina. J Comp Neurol 492:66-77.
60. Wässle H (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5:747-757.
61. White TW, Bruzzone R, Goodenough DA, Paul DL (1992) Mouse Cx50, a functional member of the connexin family of gap junction proteins, is the lens fiber protein MP70. Mol Biol Cell 3:711-720.
62. White TW, Goodenough DA, Paul DL (1998) Targeted ablation of connexin50 in mice results in microphthalmia and zonular pulverulent cataracts. J Cell Biol 143:815-825.
63. Xin D, Bloomfield SA (1999) Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. J Comp Neurol 405:75-87.
64. 2+ on signal transmission from rods and cones to bipolar cells in carp retina. Brain Res 957:136-143.
65. Zampighi GA, Plannells AM, Lin D, Takemoto D (2005) Regulation of lens cell-to-cell communication by activation of PKCgamma and disassembly of Cx50 channels. Invest Ophthalmol Vis Sci 46:3247-3255.