Unidirectional photoreceptor-to-Müller glia coupling and unique K + channel expression in caiman retina

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Zayas Santiago, Astrid ^a   Agte, Silke ^b   Rivera, Yomarie ^a   Benedikt, Jan ^a   Ulbricht, Elke ^b,d   Karl, Anett ^b   Dávila, José ^a   Savvinov, Alexey ^c   Kucheryavykh, Yuriy ^a   Inyushin, Mikhail ^a   Cubano, Luis A ^a   Pannicke, Thomas ^b   Veh, Rüdiger W ^e   Francke, Mike ^b   Verkhratsky, Alexei ^f   Eaton, Misty J ^a   Reichenbach, Andreas ^b   Skatchkov, Serguei N ^a  

^a SCHOOL OF MEDICINE   (Puerto Rico)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^f UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE AMMONIA LIGASE; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR4.1; POTASSIUM CHANNEL; POTASSIUM CHANNEL TASK 1; PROTEIN S100B; SULFORHODAMINE B; UNCLASSIFIED DRUG; VIMENTIN; GLUTAMIC ACID DERIVATIVE; KCNJ10 (CHANNEL); NERVE PROTEIN; POTASSIUM; POTASSIUM CHANNEL SUBFAMILY K MEMBER 3; TANDEM PORE DOMAIN POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAIMAN; CELL ADHESION; CELL COMMUNICATION; CELL ISOLATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GLIA; IMMUNOCHEMISTRY; MUELLER CELL; NERVE CELL; NONHUMAN; PHOTORECEPTOR CELL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA; RETINA CONE; VISION; VOLTAGE CLAMP TECHNIQUE; ANIMAL; CHANNEL GATING; CHEMISTRY; CROCODILIAN; CYTOLOGY; MACROGLIA; MEMBRANE POTENTIAL; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

ALLIGATORS AND CROCODILES; ANIMALS; EPENDYMOGLIAL CELLS; FLUORESCENT DYES; GLUTAMATES; ION CHANNEL GATING; MEMBRANE POTENTIALS; NERVE TISSUE PROTEINS; NEURONS; PHOTORECEPTOR CELLS, VERTEBRATE; POTASSIUM; POTASSIUM CHANNELS, INWARDLY RECTIFYING; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; PROTEIN STRUCTURE, TERTIARY; RETINA; SIGNAL TRANSDUCTION;

EID: 84901334734     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097155     Document Type: Article

References (108)

1. Müller H (1851) Zur Histologie der Netzhaut. Z Wissenschaft Zool 3: 234-237.
2. Newman EA, Reichenbach A (1996) The Müller cell: a functional element of the retina. Trends Neurosci 19: 307-312.
3. Bringmann A, Pannicke T, Franke M, Wiedemann P, Skatchkov SN, et al. (2006) Müller cells in the healthy and diseased retina. Prog Retin Eye Res 25: 397-424. (Pubitemid 44038611)
4. Reichenbach A, Bringmann A (2013) New functions of Müller cells. Glia 61: 651-678.
5. Pannicke T, Biedermann B, Uckermann O, Weick M, Bringmann A, et al. (2005) Physiological properties of retinal Müller glial cells from the cynomolgus monkey, Macaca fascicularis-a comparison to human Müller cells. Vision Res 45: 1781-1791. (Pubitemid 40432068)
6. Chao TI, Grosche J, Friedrich KJ, Biedermann B, Francke M, et al. (1997) Comparative studies on mammalian Müller (retinal glial) cells. J Neurocytol 26: 439-454. (Pubitemid 27382099)
7. Newman EA (1988) Potassium conductance in Müller cells of fish. Glia 1: 275-281.
8. Malchow RP, Qian HH, Ripps H (1989) gamma-Aminobutyric acid (GABA)-induced currents of skate Müller (glial) cells are mediated by neuronal-like GABAA receptors. Proc Natl Acad Sci U S A 86: 4326-4330. (Pubitemid 19154788)
9. Ball AK, McReynolds JS (1998) Localization of gap junctions and tracer coupling in retinal Müller cells. J Comp Neurol 393: 48-57. (Pubitemid 28120065)
10. Newman EA (1984) Regional specialization of retinal glial cell membrane. Nature 309: 155-157.
11. Newman EA (1985) Membrane physiology of retinal glial (Müller) cells. J Neurosci 5: 2225-2239.
12. Skatchkov SN, Vyklický L, Orkand RK (1995) Potassium currents in endfeet of isolated Müller cells from the frog retina. Glia 15: 54-64.
13. Conner JD, Detwiler PB, Sarthy PV (1985) Ionic and electrophysiological properties of retinal Müller (glial) cells of the turtle. J Physiol 362: 79-92. (Pubitemid 15122235)
14. +channel in Müller cells of the turtle (Pseudemys scripta elegans) retina. J Membr Biol 141: 239-245.
15. Linn DM, Solessio E, Perlman I, Lasater EM (1998) The role of potassium conductance in the generation of light responses in Müller cells of the turtle retina. Vis Neurosci 15: 449-458. (Pubitemid 28235802)
16. Solessio E, Linn DM, Perlman I, Lasater EM (2000) Characterization with barium of potassium currents in turtle retinal Müller cells. J Neurophysiol 83: 418-430. (Pubitemid 30039311)
17. Govardovski VI, Chkheidze NI, Zueva LV (1987) Morphofunctional study of the retina on Caiman crocodilus. Sensornye Systemy 1: 28-35.
18. Iwabe N, Hara Y, Kumazawa Y, Shibamoto K, Saito Y, et al. (2005) Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. Mol Biol Evol 22: 810-813. (Pubitemid 40471395)
19. Franze K, Grosche J, Skatchkov SN, Schinkinger S, Foja C, et al. (2007) Müller cells are living optical fibers in the vertebrate retina. Proc Natl Acad Sci U S A. 104: 8287-8292. (Pubitemid 47175480)
20. Bykov KA, Dmitriev AV, Skachkov SN (1984) Extracellular potassium in the frog retina and its light-induced changes. Fiziol Zh SSSR Im I M Sechenova 70: 1381-1387.
21. + activity changes related to electroretinogram components. I. Amphibian (I-type) retinas. J Gen Physiol 85: 885-909.
22. + activity changes related to electroretinogram components. II. Rabbit (E-type) retinas. J Gen Physiol 85: 911-931.
23. Dmitriev AV, Govardovskii VI, Schwahn HN, Steinberg RH (1999) Light-induced changes of extracellular ions and volume in the isolated chick retinapigment epithelium preparation. Vis Neurosci 16: 1157-1167. (Pubitemid 30028240)
24. Kofuji P, Biedermann B, Siddharthan V, Raap M, Iandiev I, et al. (2002) Kir potassium channel subunit expression in retinal glial cells: implications for spatial potassium buffering. Glia 39: 292-303.
25. Butt AM, Kalsi A (2006) Inwardly rectifying potassium channels (Kir) in central nervous system glia: a special role for Kir4.1 in glial functions. J Cell Mol Med 10: 33-44. (Pubitemid 44874290)
26. +buffering to cell differentiation. J Neurochem 107: 589-601.
27. + channels and gap junction coupling. Glia 60: 1192-1202.
28. Kucheryavykh YV, Kucheryavykh LY, Nichols CG, Maldonado HM, Baksi K, et al. (2007) Downregulation of Kir4.1 inward rectifying potassium channel subunits by RNAi impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 55: 274-281. (Pubitemid 46225959)
29. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD (2007) Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27: 11354-11365. (Pubitemid 47621304)
30. Buono RJ, Lohoff FW, Sander T, Sperling MR, O'Connor MJ, et al. (2004) Association between variation in the human KCNJ10 potassium ion channel gene and seizure susceptibility. Epilepsy Res 58: 175-183. (Pubitemid 38553953)
31. Scholl UI, Choi M, Liu T, Ramaekers VT, Häusler MG, et al. (2009) Seizures, sensorineural deafness, ataxia, mental retardation, and electrolyte imbalance (SeSAME syndrome) caused by mutations inKCNJ10. Proc Natl Acad Sci U S A 106: 5842-5847.
32. Bockenhauer D, Feather S, Stanescu HC, Bandulik S, Zdebik AA, et al. (2009) Epilepsy, ataxia, sensorineural deafness, tubulopathy, and KCNJ10 mutations. N Engl J Med 360: 1960-1970.
33. Inyushin M, Kucheryavykh LY, Kucheryavykh YV, Nichols CG, Buono RJ, et al. (2010) Potassium channel activity and glutamate uptake are impaired in astrocytes of seizure-susceptible DBA/2 mice. Epilepsia 51: 1707-1713.
34. Srivastava R, Aslam M, Kalluri SR, Schirmer L, Buck D, et al. (2012) Potassium channel KIR4.1 as an immune target in multiple sclerosis. N Engl J Med 367: 115-123.
35. Reichold M, Zdebik AA, Lieberer E, Rapedius M, Schmidt K, et al. (2010) KCNJ10 gene mutations causing EAST syndrome (epilepsy, ataxia, sensorineural deafness, and tubulopathy) disrupt channel function. Proc Natl Acad Sci U S A 107: 14490-14495.
36. + channel Kir4.1. Neurobiol Dis 43: 239-247.
37. Sala-Rabanal M, Kucheryavykh LY, Skatchkov SN, Eaton MJ, Nichols CG (2010) Molecular mechanisms of EAST/SeSAME syndrome mutations in Kir4.1 (KCNJ10). J Biol Chem 285: 36040-36048.
38. Pannicke T, Iandiev I, Wurm A, Uckermann O, vom Hagen F, et al. (2006) Diabetes alters osmotic swelling characteristics and membrane conductance of glial cells in rat retina. Diabetes 55: 633-639. (Pubitemid 43343219)
39. Pannicke T, Iandiev I, Uckermann O, Biedermann B, Kutzera F, et al. (2004) A potassium channel-linked mechanism of glial cell swelling in the postischemic retina. Mol Cell Neurosci 26: 493-502. (Pubitemid 38969947)
40. Olsen ML, Campbell SC, McFerrin MB, Floyd CL, Sontheimer H (2010) Spinal cord injury causes a wide-spread, persistent loss of Kir4.1 and glutamate transporter 1: benefit of 17β-oestradiol treatment. Brain 133: 1013-1025.
41. Thomzig A, Liss B, Wenzel M, Karschin C, Eaton MJ, et al. (2001) Kir 6.1 is the principal pore-forming subunit of astrocyte but not neuronal plasma membrane KATP channels. Mol Cell Neurosci 18: 671-690. (Pubitemid 34060148)
42. Eaton MJ, Skatchkov SN, Brune A, Biedermann B, Veh RW, et al. (2002) SUR 1 and Kir 6.1 subunits of KATP-channels are co-localized in retinal (Müller) glial cells. Neuroreport 13: 57-60. (Pubitemid 34102027)
43. Raap M, Biedermann B, Braun P, Milenkovic I, Skatchkov SN, et al. (2002) Diversity of Kir channel subunit mRNA expressed by retinal glial cells of the guinea-pig. Neuroreport 13: 1037-1040. (Pubitemid 34587736)
44. Skatchkov SN, Thomzig A, Eaton MJ, Biedermann B, Eulitz D, et al. (2001) Kir subfamily in frog retina: specific spatial distribution of Kir 6.1 in glial (Müller) cells. Neuroreport 12: 1437-1441 (Pubitemid 32476143)
45. Skatchkov SN, Rojas L, Eaton MJ, Orkand RK, Biedermann B, et al. (2002) Functional expression of Kir 6.1/SUR1-Katp channels in frog retinal Müller glial cells. Glia 38: 256-267.
46. Eaton MJ, Veh RW, Makarov F, Shuba YM, Reichenbach A, et al. (2004) Uneven distribution of tandem-pore potassium channels in amphibian retina. Neuroreport 15: 321-324. (Pubitemid 38297358)
47. Skatchkov SN, Eaton MJ, Shuba YM, Kucheryavykh YV, Derst C, et al. (2006) Tandem-pore domain potassium channels are functionally expressed in retinal (Müller) glial cells. Glia 53: 266-276. (Pubitemid 43221349)
48. Nichols CG (2006) KATP channels as molecular sensors of cellular metabolism. Nature 440: 470-476.
49. Glukhov AV, Uchida K, Efimov IR, Nichols CG (2013) Functional roles of KATP channel subunits in metabolic inhibition. J Mol Cell Cardiol 62: 90-98.
50. Cui Y, Giblin JP, Clapp LH, Tinker A (2001) A mechanism for ATP-sensitive potassium channel diversity: Functional coassembly of two pore-forming subunits. Proc Natl Acad Sci USA 98: 729-734. (Pubitemid 32105111)
51. Ettaiche M, Heurteaux C, Blondeau N, Borsotto M, Tinel N, et al. (2001) ATP-sensitive potassium channels (K(ATP)) in retina: a key role for delayed ischemic tolerance. Brain Res 890: 118-129. (Pubitemid 32119531)
52. +-ATP-channel- related protein complexes: potential transducers in the regulation of epithelial tight junction permeability. J Cell Sci 119: 3087-3097.
53. + channels in pancreatic B-cells. Nature 311: 271-273.
54. Shyng SL, Nichols CG (1998) Membrane phospholipid control of nucleotide sensitivity of KATP channels. Science 282: 1138-1141.
55. MacGregor GG, Dong K, Vanoye CG, Tang L, Giebisch G, et al. (2002) Nucleotides and phospholipids compete for binding to the C terminus of KATP channels. Proc Natl Acad Sci U S A 99: 2726-2731. (Pubitemid 34240528)
56. Hibino H, Horio Y, Inanobe A, Doi K, Ito M, et al. (1997) An ATP-dependent inwardly rectifying potassium channel, KAB-2 (Kir4. 1), in cochlear stria vascularis of inner ear: its specific subcellular localization and correlation with the formation of endocochlear potential. J Neurosci 17: 4711-4721. (Pubitemid 27246928)
57. Zayas-Santiago A, Agte S, Zueva L, Savvinov A, Benedikt J, et al. (2012) Morpho-physiological characterization of retinal Müller cells from the Spectacled caiman. Program No. 566.12. Neuroscience Abstracts. New Orleans, LA: Society for Neuroscience, 2012. Online.
58. + buffering. Program No. 320.08. Neuroscience Abstracts: San Diego, CA: Society for Neuroscience, 2013. Online.
59. Krishnamoorthy V, Jain V, Cherukuri P, Baloni S, Dhingra NK (2008) Intravitreal injection of fluorochrome-conjugated peanut agglutinin results in specific and reversible labeling of mammalian cones in vivo. Invest Opthalmol Vis Sci 49: 2643-2650.
60. Iandiev I, Pannicke T, Hollborn M, Wiedemann P, Reichenbach A, et al. (2008a) Localization of glial aquaporin-4 and Kir4.1 in the light-injured murine retina. Neurosci Lett 434: 317-421.
61. Iandiev I, Wurm A, Hollborn M, Wiedemann P, Grimm C, et al. (2008b) Müller cell response to blue light injury of the rat retina. Invest Ophthalmol Vis Sci 49: 3559-3567.
62. Kucheryavykh YV, Shuba YM, Antonov SM, Inyushin MY, Cubano L, et al. (2008) Complex rectification of Müller cell Kir currents. Glia 56: 775-790.
63. Benedikt J, Inyushin M, Kucheryavykh YV, Rivera Y, Kucheryavykh LY, et al. (2012) Intracellular polyamines enhance astrocytic coupling. Neuroreport 23: 1021-1025.
64. Du G, Chen X, Todorovic MS, Shu S, Kapur J, et al. (2011) TASK channel deletion reduces sensitivity to local anesthetic-induced seizures. Anesthesiology. 115: 1003-1011.
65. 2+. Neurosci Lett 155: 15-18.
66. Newman EA (1993) Inward-rectifying potassium channels in retinal glial (Müller) cells. J Neurosci 13: 3333-3345.
67. Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372: 366-369. (Pubitemid 24363439)
68. Biedermann B, Skatchkov SN, Brunk I, Bringmann A, Pannicke T, et al. (1998) Spermine/spermidine is expressed by retinal glial (Müller) cells and controls distinct K+ channels of their membrane. Glia 23: 209-220. (Pubitemid 28259719)
69. Reyes R, Duprat F, Lesage F, Fink M, Farman N, et al. (1998) Cloning and expression of a novel pH-sensitive two pore domain potassium channel from human kidney. J Biol Chem 273: 30863-30869. (Pubitemid 28533086)
70. Lesage F, Lazdunski M (2000) Molecular and functional properties of two-pore-domain potassium channels. Am J Physiol Renal Physiol 279: F793-F801.
71. Han J, Truell J, Gnatenco C, Kim D (2002) Characterization of four types of background potassium channels in rat cerebellar granule neurons. J Physiol 542: 431-444. (Pubitemid 35190305)
72. Imanaga I, Kameyama M, Irisawa H (1987) Cell-to-cell diffusion of fluorescent dyes in paired ventricular cells. Am J Physiol 252: H223-232.
73. Safranyos RGA, Caveney S, Miller JG, Petersen NO (1987) Relative roles of gap junction channels and cytoplasm in cell-to-cell diffusion of fluorescent tracers. Proc Natl Acad Sci USA 84: 2272-2276. (Pubitemid 17075853)
74. Bank M, Schacher S (1992) Segregation of presynaptic inputs on an identified target neuron in vitro: structural remodeling visualized over time. J Neurosci 12: 2960-2972.
75. Zhu H, Wu F, Schacher S (1994) Aplysia cell adhesion molecules and serotonin regulate sensory cell-motor cell interactions during early stages of synapse formation in vitro. J Neurosci 14: 6886-6900. (Pubitemid 24336363)
76. Wagner EC, Raymond PA (1991) Müller glial cells of the goldfish retina are phagocytic in vitro but not in vivo. Exp Eye Res 53: 583-589.
77. Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, et al. (2000) Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: phenotypic impact in retina. J Neurosci 20: 5733-5740. (Pubitemid 30636901)
78. Ishii M, Fujita A, Iwai K, Kusaka S, Higashi K, et al. (2003) Differential expression and distribution of Kir5.1 and Kir4.1 inwardly rectifying K+ channels in retina. Am J Physiol Cell Physiol 285: C260-267. (Pubitemid 36917840)
79. Iandiev I, Tenckhoff S, Pannicke T, Biedermann B, Hollborn M, et al. (2006) Differential regulation of Kir4.1 and Kir2.1 expression in the ischemic rat retina. Neurosci Lett 396: 97-101. (Pubitemid 43276420)
80. Connors NC, Kofuji P (2006) Potassium channel Kir4.1 macromolecular complex in retinal glial cells. Glia 53: 124-131.
81. Reichelt W, Müller T, Pastor A, Pannicke T, Orkand PM, et al. (1993) Patch-clamp recordings from Müller (glial) cell endfeet in the intact isolated retina and acutely isolated Müller cells of mouse and guinea pig. Neuroscience 57: 599-613. (Pubitemid 23350550)
82. Zahs KR, Ceelen PW (2006) Gap junctional coupling and connexin immunoreactivity in rabbit retinal glia. Vis Neurosci 23: 1-10. (Pubitemid 43376250)
83. Schwartz EA (1993) l-Glutamate conditionally modulates the K currents of Müller glial cells. Neuron 10: 1141-1149.
84. Francke M, Pannicke T, Biedermann B, Faude F, Wiedemann P, et al. (1997) Loss of inwardly rectifying potassium currents by human retinal glial cells in diseases of the eye. Glia 20: 210-218. (Pubitemid 27324307)
85. Dreher Z, Distler C, Dreher B (1994) Vitread proliferation of filamentous processes in avian Müller cells and its putative functional correlates. J Comp Neurol 350: 96-108. (Pubitemid 24351577)
86. Laurens H, Detwiler SR (1921) Studies on the retina. The structure of the retina of Alligator mississipiensis and its photomechanical changes. J exp Zool 32: 207-234.
87. Wald G, Brown PK, Kennedy D (1957) The visual system of the alligator. J Gen Physiol 40: 703-713.
88. Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science Bulletin. Bloomfield Hills, Michigan: Michigan University Press. 785 p.
89. Walls GL (1967) The vertebrate eye and its adaptive radiation. New York: Hafner.
90. Newman EA (1987) Distribution of potassium conductance in mammalian Müller (glial) cells: a comparative study. J Neurosci 7: 2423-2432.
91. + buffering conditions in Müller glial cells of rabbit retina during postnatal development. Neurosci Lett 365: 167-170.
92. Pannicke T, Bringmann A, Reichenbach A (2002) Electrophysiological characterization of retinal Müller glial cells from mouse during postnatal development: comparison with rabbit cells. Glia 38: 268-272.
93. Bringmann A, Biedermann B, Reichenbach A (1999) Expression of potassium channels during postnatal differentiation of rabbit Müller glial cells. Eur J Neurosci 11: 2883-2896. (Pubitemid 29364205)
94. + channels in retinal glial cells is associated with a decrease of osmotic cell swelling. Glia.54: 411-423.
95. Zhou M, Schools GP, Kimelberg HK (2006) Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J Neurophysiol 95: 134-143. (Pubitemid 44698923)
96. + channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J Neurosci 29: 7474-7488.
97. + channels and aquaporins 4 and 5 in autoimmune uveitis indicates misbalance in Müller glial cell-dependent ion and water homeostasis. Glia 59: 697-707.
98. Thompson DA, Feather S, Stanescu HC, Freudenthal B, Zdebik AA, et al. (2011) Altered electroretinograms in patients with KCNJ10 mutations and EAST syndrome. J Physiol 589: 1681-1689.
99. Morton MJ, Chipperfield S, Abohamed A, Sivaprasadarao A, Hunter M (2005) Na(+)-induced inward rectification in the two-pore domain K(+) channel, TASK-2. Am J Physiol Renal Physiol. 288: F162-169. (Pubitemid 40038688)
100. Nagelhus EA, Veruki ML, Torp R, Haug FM, Laake JH, et al. (1998) Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Müller cells and fibrous astrocytes. J Neurosci. 18(7): 2506-2519.
101. Amiry-Moghaddam M, Ottersen OP (2005) The molecular basis of water transport in the brain. Nat Rev Neurosci. 4(12): 991-1001.
102. Hoomann T, Jahnke N, Horner A, Keller S, Pohl P (2013) Filter gate closure inhibits ion but not water transport through potassium channels. Proc Natl Acad Sci U S A. 110(26): 10842-10847.
103. Janssen-Bienhold U, Dermietzel R, Weiler R (1998) Distribution of connexin43 immunoreactivity in the retinas of different vertebrates. J Comp Neurol. 396: 310-321. (Pubitemid 28264846)
104. Zahs KR, Kofuji P, Meier C, Dermietzel R (2003) Connexin immunoreactivity in glial cells of the rat retina. J Comp Neurol 455: 531-546. (Pubitemid 36043654)
105. Giblin LJ, Christensen BN (1997) Connexin43 immunoreactivity in the catfish retina. Brain Res 755: 146-150. (Pubitemid 27192009)
106. Robinson SR, Hampson EC, Munro MN, Vaney DI (1993) Unidirectional coupling of gap junctions between neuroglia. Science 262: 1072-1074. (Pubitemid 24035050)
107. Zahs KR, Newman EA (1997) Asymmetric gap junctional coupling between glial cells in the rat retina. Glia 20: 10-22. (Pubitemid 27207004)
108. Zahs KR (1998) Heterotypic coupling between glial cells of the mammalian central nervous system. Glia 24: 85-96.