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Characterization of connexin36 gap junctions in the human outer retina

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Abstract

Retinal connexins (Cx) form gap junctions (GJ) in key circuits that transmit average or synchronize signals. Expression of Cx36, -45, -50 and -57 have been described in many species but there is still a disconcerting paucity of information regarding the Cx makeup of human retinal GJs. We used well-preserved human postmortem samples to characterize Cx36 GJ constituent circuits of the outer plexiform layer (OPL). Based on their location, morphometric characteristics and co-localizations with outer retinal neuronal markers, we distinguished four populations of Cx36 plaques in the human OPL. Three of these were comprised of loosely scattered Cx36 plaques; the distalmost population 1 formed cone-to-rod GJs, population 2 in the mid-OPL formed cone-to-cone GJs, whereas the proximalmost population 4 likely connected bipolar cell dendrites. The fourth population (population 3) of Cx36 plaques conglomerated beneath cone pedicles and connected dendritic tips of bipolar cells that shared a common presynaptic cone. Overall, we show that the human outer retina displays a diverse cohort of Cx36 GJ that follows the general mammalian scheme and display a great functional diversity.

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Acknowledgments

The authors thank to Zsuzsanna Vidra for her technical help and are grateful to Dr. Mark Eyre for the assistance with the English language. The authors are thankful for providing the antibodies: Noga Vardi (mGluR6), Wilhelm Koch (recoverin), Alán Alpár (guinea pig calbindin), Norbert Hájos (GluA4N). Supported by OTKA K105247 to B.V. and OTKA 73000 Á.S. This research was supported by the European Union and the State of Hungary, co-financed by the European Social Fund in the framework of TÁMOP-4.2.4.A/2-11/1-2012-0001 ‘National Excellence Program’.to B.V. Finally, B.V. was also supported by the Hungarian Brain Research Program (KTIA_NAP_13-2-2015-0008).

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Authors and Affiliations

  1. Department of Anatomy, Histology and Embryology, Semmelweis University, Budapest, 1094, Hungary

    Orsolya Kántor & Emese Pálfi

  2. Department of Theory, Wigner Research Center for Physics of the Hungarian Academy of Sciences, Budapest, 1121, Hungary

    Zsigmond Benkő

  3. Semmelweis University School of Ph.D. Studies, Budapest, 1085, Hungary

    Zsigmond Benkő

  4. Department of Ophthalmology, Semmelweis University, Budapest, 1085, Hungary

    Anna Énzsöly & János Németh

  5. Department of Human Morphology and Developmental Biology, Semmelweis University, Budapest, 1094, Hungary

    Anna Énzsöly, Csaba Dávid, Arnold Szabó, Ágoston Szél & Ákos Lukáts

  6. Life Imaging Center, Center for Biological Systems Analysis, Albert-Ludwigs University, 79104, Freiburg, Germany

    Angela Naumann & Roland Nitschke

  7. BIOSS Centre for Biological Signalling Studies, Albert-Ludwigs-University Freiburg, 79104, Freiburg, Germany

    Angela Naumann & Roland Nitschke

  8. Department of Biophysics, University of Pécs, Pécs, 7624, Hungary

    József Orbán & Miklós Nyitrai

  9. János Szentágothai Research Center, University of Pécs, Ifjúság str. 6, 7624, Pécs, Hungary

    József Orbán, Miklós Nyitrai & Béla Völgyi

  10. MTA-PTE NAP B Retinal Electrical Synapses Research Group, Pécs, 7624, Hungary

    Béla Völgyi

  11. Department of Experimental Zoology and Neurobiology, University of Pécs, Pécs, 7624, Hungary

    Béla Völgyi

  12. Department of Ophthalmology, New York University Langone Medical Center, New York, NY, 10016, USA

    Béla Völgyi

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  1. Orsolya Kántor
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  2. Zsigmond Benkő
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  3. Anna Énzsöly
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  5. Angela Naumann
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  7. Arnold Szabó
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  8. Emese Pálfi
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  9. József Orbán
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  10. Miklós Nyitrai
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  11. János Németh
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  12. Ágoston Szél
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  13. Ákos Lukáts
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  14. Béla Völgyi
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Correspondence to Béla Völgyi.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee (number of permission: TUKEB 58/2006) and with the 1964 Helsinki declaration and its later amendments.

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Kántor, O., Benkő, Z., Énzsöly, A. et al. Characterization of connexin36 gap junctions in the human outer retina. Brain Struct Funct 221, 2963–2984 (2016). https://doi.org/10.1007/s00429-015-1082-z

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