Expression and function of the neuronal gap junction protein connexin 36 in developing mammalian retina

Journal of Comparative Neurology

Volumn 493, Issue 2, 2005, Pages 309-320

  Hansen, Kristi A ^a   Torborg, Christine L ^a,b   Elstrott, Justin ^a   Feller, Marla B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Amacrine cells; Bipolar cells; Gap junctions; Retinal ganglion cells; Retinal waves

Indexed keywords

4 AMINOBUTYRIC ACID; BETA GALACTOSIDASE; CONNEXIN 36; GAP JUNCTION PROTEIN;

ANIMAL TISSUE; ARTICLE; EYE DEVELOPMENT; GAP JUNCTION; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MICROSCOPY; MOUSE; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA GANGLION CELL;

ANIMALS; BETA-GALACTOSIDASE; CONNEXINS; GAP JUNCTIONS; GENES, REPORTER; MICE; MICE, KNOCKOUT; NEURONS; PHOTOTRANSDUCTION; RETINA;

EID: 27944508685     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20759     Document Type: Article

References (70)

1. Bansal A, Singer JH, Hwang BJ, Xu W, Beaudet A, Feller MB. 2000. Mice lacking specific nAChR subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON/OFF circuits in the inner retina. J Neurosci 20:7672-7681.
2. Belluardo N, Mudo G, Trovato-Salinaro A, Le Gurun S, Charollais A, Serre-Beinier V, Amato G, Haefliger JA, Meda P, Condorelli DF. 2000. Expression of connexin36 in the adult and developing rat brain. Brain Res 865:121-138.
3. Ben-Ari Y, Khalilov I, Represa A, Gozlan H. 2004. Interneurons set the tune of developing networks. Trends Neurosci 27:422-427.
4. Bentley D, Keshishian H. 1982. Pathfinding by peripheral pioneer neurons in grasshoppers. Science 218:1082-1087.
5. Bittman K, Owens DF, Kriegstein AR, LoTurco JJ. 1997. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J Neurosci 17:7037-7044.
6. Buhl DL, Harris KD, Hormuzdi SG, Monyer H, Buzsaki G. 2003. Selective impairment of hippocampal gamma oscillations in connexin-36 knockout mouse in vivo. J Neurosci 23:1013-1018.
7. 2+ transients and their transmission in the developing chick retina. Curr Biol 8:283-286.
8. 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.
9. Condorelli DF, Belluardo N, Trovato-Salinaro A, Mudo G. 2000. Expression of Cx36 in mammalian neurons. Brain Res Brain Res Rev 32:72-85.
10. Connors BW, Long MA. 2004. Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393-418.
11. Cusato K, Bosco A, Rozental R, Guimaraes CA, Reese BE, Linden R, Spray DC. 2003. Gap junctions mediate bystander cell death in developing retina. J Neurosci 23:6413-6422.
12. Deans MR, Paul DL. 2001. Mouse horizontal cells do not express connexin26 or connexin36. Cell Commun Adhes 8:361-366.
13. 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.
14. 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.
15. Degen J, Meier C, Van Der Giessen RS, Sohl G, Petrasch-Parwez E, Urschel S, Dermietzel R, Schilling K, De Zeeuw CI, Willecke K. 2004. Expression pattern of lacZ reporter gene representing connexin36 in transgenic mice. J Comp Neurol 473:511-525.
16. Demas J, Eglen SJ, Wong RO. 2003. Developmental loss of synchronous spontaneous activity in the mouse retina is independent of visual experience. J Neurosci 23:2851-2860.
17. Famiglietti EV Jr, Kolb H. 1975. A bistratified amacrine cell and synaptic cirucitry in the inner plexiform layer of the retina. Brain Res 84:293-300.
18. 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.
19. 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.
20. Feller MB. 2002. The role of nAChR-inediated spontaneous retinal activity in visual system development. J Neurobiol 53:556-567.
21. Feller MB, Wellis DP, Stellwagen D, Werblin FS, Shatz CJ. 1996. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272:1182-1187.
22. Firth S, Wang C, Feller M. 2005. Retinal waves: mechanisms and function in visual system development. Cell Calcium (in press).
23. Grubb MS, Thompson ID. 2004. The influence of early experience on the development of sensory systems. Curr Opin Neurobiol 14:503-512.
24. 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.
25. Gunhan-Agar E, Kahn D, Chalupa LM. 2000. Segregation of On and off bipolar cell axonal arbors in the absence of retinal ganglion cells. J Neurosci 20:306-314.
26. Hanson MG, Landmesser LT. 2003. Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J Neurosci 23:587-600.
27. Haverkamp S, Wassle H. 2000. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23.
28. Hidaka S, Kato T, Miyachi E. 2002. Expression of gap junction connexin36 in adult rat retinal ganglion cells. J Integr Neurosci 1:3-22.
29. Hidaka S, Akahori Y, Kurosawa Y. 2004. Dendrodendritic electrical synapses between mammalian retinal ganglion cells. J Neurosci 24:10553-10567.
30. 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.
31. Howell BW, Gertler FB, Cooper JA. 1997. Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J 16:121-132.
32. Jeon CJ, Strettoi E, Masland RH. 1998. The major cell populations of the mouse retina. J Neurosci 18:8936-8946.
33. Kandler K, Katz LC. 1998. Coordination of neuronal activity in developing visual cortex by gap junction-mediated biochemical communication. J Neurosci 18:1419-1427.
34. Lin JH, Weigel H, Cotrina ML, Liu S, Bueno E, Hansen AJ, Hansen TW, Goldman S, Nedergaard M. 1998. Gap-junction-mediated propagation and amplification of cell injury. Nat Neurosci 1:494-500.
35. Long MA, Deans MR, Paul DL, Connors BW. 2002. Rhythmicity without synchrony in the electrically uncoupled inferior olive. J Neurosci 22: 10898-10905.
36. 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.
37. Meister M, Wong RO, Baylor DA, Shatz CJ. 1991. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252:939-943.
38. Meister M, Pine J, Baylor DA. 1994. Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods 51:95-106.
39. Menger N, Pow DV, Wassle H. 1998. Glycinergic amacrine cells of the rat retina. J Comp Neurol 401:34-46.
40. Mills SL, O'Brien JJ, Li W, O'Brien J, Massey SC. 2001. Rod pathways in the mammalian retina use connexin 36. J Comp Neurol 436:336-350.
41. Moon JI, Kim IB, Gwon JS, Park MH, Kang TH, Lim EJ, Choi KR, Chun MH. 2005. Changes in retinal neuronal populations in the DBA/2J mouse. Cell Tissue Res 320:51-59 [Epub 2005 Feb 2016].
42. Naus CC, Bani-Yaghoub M. 1998. Gap junctional communication in the developing central nervous system. Cell Biol Int 22:751-763.
43. Peinado A, Yuste R, Katz LC. 1993. Gap junctional communication and the development of local circuits in neocortex. Cereb Cortex 3:488-498.
44. Penn AA, Riquelme PA, Feller MB, Shatz CJ. 1998. Competition in retinogeniculate patterning driven by spontaneous activity. Science 279; 2108-2112.
45. Personius KE, Balice-Gordon RJ. 2001. Loss of correlated motor neuron activity during synaptic competition at developing neuromuscular synapses. Neuron 31:395-408.
46. 3H)glycine-accumulating amacrine cells in the cat retina. J Comp Neurol 233:473-480.
47. Pow DV, Hendrickson AE. 2000. Expression of glycine and the glycine transporter glyt-1 in the developing rat retina. Vis Neurosci 17:1-9.
48. Rash JE, Staines WA, Yasumura T, Patel D, Furman CS, Stelmack GL, Nagy JI. 2000. Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin-36 but not connexin-32 or connexin-43. Proc Natl Acad Sci U S A 97:7573-7578.
49. Rice DS, Curran T. 2000. Disabled-1 is expressed in type AII amacrine cells in the mouse retina. J Comp Neurol 424:327-338.
50. Saint-Amant L, Drapeau P. 2001. Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron 31:1035-1046.
51. Schubert T, Degen J, Willecke K, Hormuzdi SG, Monyer H, Weiler R. 2005. Connexin36 mediates gap junctional coupling of alpha-ganglion cells in mouse retina. J Comp Neurol 485:191-201.
52. Sernagor E, Eglen SJ, Wong RO. 2001. Development of retinal ganglion cell structure and function. Prog Ret Eye Res 20:139-174.
53. Singer JH, Mirotznik RR, Feller MB. 2001. Potentiation of L-type calcium channels reveals nonsynaptic mechanisms that correlate spontaneous activity in the developing mammalian retina. J Neurosci 21:8514-8522.
54. 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.
55. Sohl G, Guldenagel M, Traub O, Willecke K. 2000. Connexin expression in the retina. Brain Res Brain Res Rev 32:138-145.
56. Syed MM, Lee S, He S, Zhou ZJ. 2004a. Spontaneous waves in the ventricular zone of developing mammalian retina. J Neurophysiol 91: 1999-2009 [Epub 2003 Dec 1917].
57. Syed MM, Lee S, Zheng J, Zhou ZJ. 2004b. Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol 560:533-549 [Epub 2004 Aug 2012].
58. Torborg C, Hansen K, Feller M. 2005. High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nat Neurosci 8:72-78.
59. Vaney DI, Nelson JC, Pow DV. 1998. Neurotransmitter coupling through gap junctions in the retina. J Neurosci 18:10594-10602.
60. Veruki ML, Hartveit E. 2002a. AII (Rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33:935-946.
61. Veruki ML, Hartveit E. 2002b. Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. J Neurosci 22:10558-10566.
62. Vessey JP, Lalonde MR, Mizan HA, Welch NC, Kelly ME, Barnes S. 2004. Carbenoxolone inhibition of voltage-gated Ca channels and synaptic transmission in the retina. J Neurophysiol 92:1252-1256 [Epub 2004 Mar 1217].
63. Wong RO, Meister M, Shatz CJ. 1993. Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11:923-938.
64. Wong RO, Chernjavsky A, Smith SJ, Shatz CJ. 1995. Early functional neural networks in the developing retina. Nature 374:716-718.
65. Wong WT, Sanes JR, Wong ROL. 1998. Developmentally regulated spontaneous activity in the embryonic chick retina. J Neurosci 18:8839-8852.
66. Yuste R, Nelson DA, Rubin WW, Katz LC. 1995. Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14:7-17.
67. Zhang M, Xin H, Roon P, Atherton SS. 2005. Infection of retinal neurons during murine cytomegalovirus retinitis. Invest Ophthalmol Vis Sci 46:2047-2055.
68. Zheng JJ, Lee S, Zhou ZJ. 2004. A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44:851-864.
69. Zhou ZJ. 2001a. A critical role of the strychnine-sensitive glycinergic system in spontaneous retinal waves of the developing rabbit. J Neurosci 21:5158-5168.
70. Zhou ZJ. 2001b. The function of the cholinergic system in the developing mammalian retina. Prog Brain Res 131:599-613.