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

Journal of Neuroscience

Volumn 25, Issue 3, 2005, Pages 566-576

  Maxeiner, Stephan ^a   Dedek, Karin ^b   Janssen Bienhold, Ulrike ^b   Ammermüller, Josef ^b   Brune, Hendrik ^a   Kirsch, Taryn ^b   Pieper, Mario ^b   Degen, Joachim ^a   Krüger, Olaf ^a   Willecke, Klaus ^a   Weiler, Reto ^b  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF OLDENBURG   (Germany)

Author keywords

Adaptation; Connexin45; Electroretinogram; Gap junction; Retina; Rod pathway

Indexed keywords

CONNEXIN 36; CONNEXIN 45; ENHANCED GREEN FLUORESCENT PROTEIN;

A WAVE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B WAVE; CELL DISRUPTION; CHEMICAL LABELING; CONTROLLED STUDY; ELECTRORETINOGRAPHY; GENE DELETION; MICROINJECTION; MOUSE; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA NERVE CELL; RETINA ROD; VISUAL IMPAIRMENT;

AMACRINE CELLS; ANIMALS; CONES (RETINA); CONNEXINS; ELECTRORETINOGRAPHY; EYE PROTEINS; GENES, REPORTER; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; INTEGRASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; PHOTOTRANSDUCTION; RETINA; RODS (RETINA);

EID: 19944433958     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3232-04.2005     Document Type: Article

References (50)

1. Buchholz F, Angrand PO, Stewart AF (1998) Improved properties of FLP recombinase evolved by cycling mutagenesis. Nat Biotechnol 16:657-662.
2. 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.
3. Eckardt D, Theis M, Doring B, Speidel D, Willecke K, Ott I (2004) Spontaneous ectopic recombination in cell-type-specific Cre mice removes 10xP-flanked marker cassettes in vivo. Genesis 38:159-165.
4. A receptors of retinal dopaminergic neurons. J Neurophysiol 84:1697-1707.
5. 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.
6. Feigenspan A, Janssen-Bienhold U, Hormudzdi S, Monyer H, Degen J, Söhl G, Willecke K, Ammermüller J, Weiler R (2004) Expression of connexin36 in cone pedicles and OFF-cone bipolar cells of the mouse retina. J Neurosci 24:3325-3334.
7. Ghosh KK, Bujan S, Haverkamp S, Feigenspan A, Wässle H (2004) Types of bipolar cells in the mouse retina. J Comp Neurol 469:70-82.
8. Goodenough DA, Paul DL (2003) Beyond the gap: functions of unpaired connexon channels. Nat Rev Mol Cell Biol 4:285-294.
9. Greferath U, Grunert U, Wässle H (1990) Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. J Comp Neurol 301:433-442.
10. Güldenagel M, Söhl 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.
11. Güldenagel M, Ammermüller J, Feigenspan A, Teubner B, Degen J, Söhl G, Willecke K, Weiler R (2001) Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin36. J Neurosci 21:6036-6044.
12. Haverkamp S, Wässle H (2000) Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23.
13. Hennemann H, Schwarz HJ, Willecke K (1992) Characterization of gap junction genes expressed in F9 embryonic carcinoma cells: molecular cloning of mouse connexin31 and -45 cDNAs. Eur J Cell Biol 57:51-58.
14. Hombach S, Janssen-Bienhold U, Söhl G, Schubert T, Büssow 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.
15. Horst M, Harth N, Hasilik A (1991) Biosynthesis of glycosylated human lysozyme mutants. J Biol Chem 266:13914-13919.
16. Jeon CJ, Strettoi E, Masland RH (1998) The major cell populations of the mouse retina. J Neurosci 18:8936-8946.
17. 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.
18. Knapp AG, Schiller PH (1984) The contribution of on-bipolar cells to the electroretinogram of rabbits and monkeys. A study using 2-amino-4- phosphonobutyrate (APB). Vision Res 24:1841-1846.
19. Krüger O, Plum A, Kim JS, Winterhager E, Maxeiner S, Hallas G, Kirchhoff S, Traub O, Lamers WH, Willecke K (2000) Defective vascular development in connexin 45-deficient mice. Development 127:4179-4193.
20. Kumai M, Nishii K, Nakamura K, Takeda N, Suzuki M, Shibata Y (2000) Loss of connexin45 causes a cushion defect in early cardiogenesis. Development 127:3501-3512.
21. Lallemand Y, Luria V, Haffner-Krausz R, Lonai P (1998) Maternally expressed PGK-Cre transgene as a tool for early and uniform activation of the Cre site-specific recombinase. Transgenic Res 7:105-112.
22. Magin TM, McWhir J, Melton DW (1992) A new mouse embryonic stem cell line with good germ line contribution and gene targeting frequency. Nucleic Acids Res 20:3795-3796.
23. Massey SC, Mills SL (1999) Gap junctions between AII amacrine cells and calbindin-positive bipolar cells in the rabbit retina. Vis Neurosci 16:1181-1189.
24. Masu M, Iwakabe H, Tagawa Y, Miyoshi T, Yamashita M, Fukuda Y, Sasaki H, Hiroi K, Nakamura Y, Shigemoto R, Takada M, Nakamura K, Nakao K, Katsuki M, Nakanishi S (1995) Specific deficit of the ON response in visual transmission by targeted disruption of the mGluRo gene. Cell 80:757-765.
25. Meyers EN, Lewandoski M, Martin GR (1998) An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 18:136-141.
26. Mills SL, Massey SC (1995) Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377:734-737.
27. 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.
28. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, Nakanishi S (1993) Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J Biol Chem 268:11868-11873.
29. Nakatani K, Tamura T, Yau KW (1991) Light adaptation in retinal rods of the rabbit and two other nonprimate mammals. J Gen Physiol 97:413-435.
30. Nishii K, Kumai M, Egashira K, Miwa T, Hashizume K, Miyano Y, Shibata Y (2003) Mice lacking connexin45 conditionally in cardiac myocytes display embryonic lethality similar to that of germline knockout mice without endocardial cushion defect. Cell Commun Adhes 10:365-369.
31. Peachey NS, Goto Y, al-Ubaidi MR, Naash MI (1993) Properties of the mouse cone-mediated electroretinogram during light adaptation. Neurosci Lett 162:9-11.
32. Pottek M, Hoppenstedt W, Janssen-Bienhold U, Schultz K, Perlman I, Weiler R (2003) Contribution of connexin26 to electrical feedback inhibition in the turtle retina. J Comp Neurol 466:468-477.
33. Raviola E, Gilula NB (1973) Gap junctions between photoreceptor cells in the vertebrate retina. Proc Natl Acad Sci USA 70:1677-1681.
34. Rodríguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, Stewart AF, Dymecki SM (2000) High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 25:139-140.
35. Söhl G, Willecke K (2003) An update on connexin genes and their nomenclature in mouse and man. Cell Commun Adhes 10:173-180.
36. 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.
37. Steinberg RH, Frishman LJ, Sieving PA (1991) Progress in retinal research. Oxford: Pergamon.
38. Steiner E, Ebihara L (1996) Functional characterization of canine connexin45. J Membr Biol 150:153-161.
39. Stockton RA, Slaughter MM (1989) B-wave of the electroretinogram. A reflection of ON bipolar cell activity. J Gen Physiol 93:101-122.
40. Strettoi E, Raviola E, Dacheux RF (1992) Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. J Comp Neurol 325:152-168.
41. Teubner B, Degen I, Söhl G, Güldenagel 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.
42. Theis M, Magin TM, Plum A, Willecke K (2000) General or cell type-specific deletion and replacement of connexin-coding DNA in the mouse. Methods 20:205-218.
43. Trexler EB, Li W, Mills SL, Massey SC (2001) Coupling from AII amacrine cells to ON cone bipolar cells is bidirectional. J Comp Neurol 437:408-422.
44. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99-103.
45. Vaney DI (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci Lett 125:187-190.
46. Vaney DI, Nelson JC, Pow DV (1998) Neurotransmitter coupling through gap junctions in the retina. J Neurosci 18:10594-10602.
47. Veruki ML, Hartveit E (2002) Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. J Neurosci 22:10558-10566.
48. Wachtmeister L, Dowling JE (1978) The oscillatory potentials of the mud-puppy retina. Invest Ophthalmol Vis Sci 17:1176-1188.
49. Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Güldenagel M, Deutsch U, Söhl G (2002) Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem 383:725-737.
50. Xin D, Bloomfield SA (1999) Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina. Vis Neurosci 16:653-665.