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A Szentágothai János Kutatóközpont a PTE korszerű, nemzetközi tudományszervezési és menedzsment normák szerint kialakított új intézménye, amely az élettudományi, élettelen természettudományi, valamint környezettudományi oktatás...

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Retinal Neurobiology Rresearch Group

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1. Retinal electrical synapses team: Dr. Béla Völgyi, Dr. Tamás Kovács-Öller, Alma Ganczer, Ádám Tengölics, Gergely Szarka, Márton Balogh

Over 85% of the information perceived by our nervous system is processed by the retina, thus it is essential to understand how the retinal neuronal hyper-network works. Electrical synapses have been known for some 40 years, however their crucial role in visual information processing has only become obvious in recent years. Our team performs experiments to show that electrically coupled retinal neuronal networks play important roles in higher visual functions. We examine the expressional changes of the gap junction forming connexin proteins during the postnatal development and/or induced by changes in the environment. Our work particularly focuses on those inner retinal gap junctions that are formed by ganglion and amacrine cells (ganglion-ganglion, amacrine-amacrine and amacrine-ganglion) and participate in the synchronization of ganglion cell action potentials. We study how such ganglion cell population activity encodes certain visual patterns or visual cues. We also study how the function of electrical and chemical synapses affect each other and if they interfere and/or cooperate to serve signaling. Results of our research will contribute to algorithms for the stimulation of retinal prostheses and/or to provide data to design high performance bionic eyes for robotics.

Alumni: László Albert, Gábor Debertin PhD, Anikó Óhidi-Légmán, Erica Popovich, Adrienn Szabó, Dániel Varga

2. Retinal signalization team: Dr. Róbert Gábriel, Dr. Andrea Kovács-Valasek

Our research focus is to expand our knowledge on the mechanisms of metabolic retinal degenerations by exploiting experimental work with animal models. We explore how metabolic mechanisms that mediate human retinal degenerations induce retinal cell loss, and which biochemical signaling pathways are involved in mechanisms that eventually impair vision. Our results will reveal the potential rescue mechanisms to avoid retinal degeneration by blocking the degeneration pathways or by enhancing mechanisms that serve neuronal protection. The knowledge on this latter issue will allow us to test and design new pharmacological compounds. Throughout these experiments we will also gain information on the mechanisms of retinal information processing, neuronal degeneration and neuronal protection.



Dr. Róbert Gábriel
professor
gabriel@ttk.pte.hu
Dr. Tamás Kovács-Öller
research fellow

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Andrea Kovács-Valasek
assistant research fellow

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Alma Ganczer
PhD student

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Ádám Jonatán Tengölics
PhD student

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Gergely Szarka
researcher

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Márton Balogh
researcher

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Kristóf Fülöp
student

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Boglárka Balogh
student

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Retinal electrical synapses team:

Kovacs-Oller T, Ivanova E, Bianchimano P, Sagdullaev BT. The pericyte connectome: spatial precision of neurovascular coupling is driven by selective connectivity maps of pericytes and endothelial cells and is disrupted in diabetes. Cell Discov 639 (2020). https://doi.org/10.1038/s41421-020-0180-0

Kovács-Öller T, Ivanova E, Szarka G, Tengölics ÁJ, Völgyi B, Sagdullaev BT. Imatinib Sets Pericyte Mosaic in the Retina. Int J Mol Sci. 2020 Apr 5;21(7):2522. doi: 10.3390/ijms21072522. PMID: 32260484; PMCID: PMC7177598.

Kovács-Öller T, Szarka G, Tengölics ÁJ, Ganczer A, Balogh B, Szabó-Meleg E, Nyitrai M, Völgyi B. Spatial Expression Pattern of the Major Ca2+-Buffer Proteins in Mouse Retinal Ganglion Cells. Cells. 2020 Mar 25;9(4):792. doi: 10.3390/cells9040792. PMID: 32218175; PMCID: PMC7226302.

Tengölics ÁJ, Szarka G, Ganczer A, Szabó-Meleg E, Nyitrai M, Kovács-Öller T, Völgyi B. Response Latency Tuning by Retinal Circuits Modulates Signal Efficiency. Sci Rep. 2019 Oct 22;9(1):15110. doi: 10.1038/s41598-019-51756-y. PMID: 31641196; PMCID: PMC6806000.

Völgyi B, Kenyon GT, Marshak DW, Sagdullaev B. Editorial: Encoding Visual Features by Parallel Ganglion Cell Initiated Pathways in the Healthy, Diseased and Artificial Retina. Front Cell Neurosci. 2019 May 24;13:229. doi: 10.3389/fncel.2019.00229. PMID: 31178700; PMCID: PMC6542953.

Telkes I, Kóbor P, Orbán J, Kovács-Öller T, Völgyi B, Buzás P. Connexin-36 distribution and layer-specific topography in the cat retina. Brain Struct Funct. 2019 Jul;224(6):2183-2197. doi: 10.1007/s00429-019-01876-y. Epub 2019 Jun 6. PMID: 31172263; PMCID: PMC6591202.

Kovács-Öller T, Szarka G, Ganczer A, Tengölics Á, Balogh B, Völgyi B. Expression of Ca2+-Binding Buffer Proteins in the Human and Mouse Retinal Neurons. Int J Mol Sci. 2019 May 7;20(9):2229. doi: 10.3390/ijms20092229. PMID: 31067641; PMCID: PMC6539911.

Kántor O, Szarka G, Benkő Z, Somogyvári Z, Pálfi E, Baksa G, Rácz G, Nitschke R, Debertin G, Völgyi B. Strategic Positioning of Connexin36 Gap Junctions Across Human Retinal Ganglion Cell Dendritic Arbors. Front Cell Neurosci. 2018 Nov 22;12:409. doi: 10.3389/fncel.2018.00409. PMID: 30524239; PMCID: PMC6262005.

Ganczer A, Balogh M, Albert L, Debertin G, Kovács-Öller T, Völgyi B. Transiency of retinal ganglion cell action potential responses determined by PSTH time constant. PLoS One. 2017 Sep 12;12(9):e0183436. doi: 10.1371/journal.pone.0183436. PMID: 28898257; PMCID: PMC5595288.

Kovács-Öller T, Debertin G, Balogh M, Ganczer A, Orbán J, Nyitrai M, Balogh L, Kántor O, Völgyi B. Connexin36 Expression in the Mammalian Retina: A Multiple-Species Comparison. Front Cell Neurosci. 2017 Mar 9;11:65. doi: 10.3389/fncel.2017.00065. PMID: 28337128; PMCID: PMC5343066.

Kántor O, Varga A, Nitschke R, Naumann A, Énzsöly A, Lukáts Á, Szabó A, Németh J, Völgyi B. Bipolar cell gap junctions serve major signaling pathways in the human retina. Brain Struct Funct. 2017 Aug;222(6):2603-2624. doi: 10.1007/s00429-016-1360-4. Epub 2017 Jan 10. PMID: 28070649.

Pan F, Toychiev A, Zhang Y, Atlasz T, Ramakrishnan H, Roy K, Völgyi B, Akopian A, Bloomfield SA. Inhibitory masking controls the threshold sensitivity of retinal ganglion cells. J Physiol. 2016 Nov 15;594(22):6679-6699. doi: 10.1113/JP272267. Epub 2016 Aug 2. PMID: 27350405; PMCID: PMC5108909.

Kántor O, Mezey S, Adeghate J, Naumann A, Nitschke R, Énzsöly A, Szabó A, Lukáts Á, Németh J, Somogyvári Z, Völgyi B. Calcium buffer proteins are specific markers of human retinal neurons. Cell Tissue Res. 2016 Jul;365(1):29-50. doi: 10.1007/s00441-016-2376-z. Epub 2016 Feb 22. PMID: 26899253.

Kántor O, Cserpán D, Völgyi B, Lukáts Á, Somogyvári Z. The Retinal TNAP. Subcell Biochem. 2015;76:107-23. doi: 10.1007/978-94-017-7197-9_6. PMID: 26219709.

Kántor O, Benkő Z, Énzsöly A, Dávid C, Naumann A, Nitschke R, Szabó A, Pálfi E, Orbán J, Nyitrai M, Németh J, Szél Á, Lukáts Á, Völgyi B. Characterization of connexin36 gap junctions in the human outer retina. Brain Struct Funct. 2016 Jul;221(6):2963-84. doi: 10.1007/s00429-015-1082-z. Epub 2015 Jul 15. PMID: 26173976.

Debertin G, Kántor O, Kovács-Öller T, Balogh L, Szabó-Meleg E, Orbán J, Nyitrai M, Völgyi B. Tyrosine hydroxylase positive perisomatic rings are formed around various amacrine cell types in the mammalian retina. J Neurochem. 2015 Aug;134(3):416-28. doi: 10.1111/jnc.13144. Epub 2015 Jun 3. PMID: 25940543.

Kántor O, Varga A, Tóth R, Énzsöly A, Pálfi E, Kovács-Öller T, Nitschke R, Szél Á, Székely A, Völgyi B, Négyessy L, Somogyvári Z, Lukáts Á. Stratified organization and disorganization of inner plexiform layer revealed by TNAP activity in healthy and diabetic rat retina. Cell Tissue Res. 2015 Feb;359(2):409-421. doi: 10.1007/s00441-014-2047-x. Epub 2014 Nov 20. PMID: 25411053.

Kovács-Öller T, Raics K, Orbán J, Nyitrai M, Völgyi B. Developmental changes in the expression level of connexin36 in the rat retina. Cell Tissue Res. 2014 Nov;358(2):289-302. doi: 10.1007/s00441-014-1967-9. Epub 2014 Aug 12. PMID: 25110193.

Akopian A, Atlasz T, Pan F, Wong S, Zhang Y, Völgyi B, Paul DL, Bloomfield SA. Gap junction-mediated death of retinal neurons is connexin and insult specific: a potential target for neuroprotection. J Neurosci. 2014 Aug 6;34(32):10582-91. doi: 10.1523/JNEUROSCI.1912-14.2014. PMID: 25100592; PMCID: PMC4200109.

Kántor O, Varga A, Kovács-Öller T, Énzsöly A, Balogh L, Baksa G, Szepessy Z, Fonta C, Roe AW, Nitschke R, Szél Á, Négyessy L, Völgyi B, Lukáts Á. TNAP activity is localized at critical sites of retinal neurotransmission across various vertebrate species. Cell Tissue Res. 2014 Oct;358(1):85-98. doi: 10.1007/s00441-014-1944-3. Epub 2014 Jul 3. PMID: 24988913.

Völgyi B, Pan F, Paul DL, Wang JT, Huberman AD, Bloomfield SA. Gap junctions are essential for generating the correlated spike activity of neighboring retinal ganglion cells. PLoS One. 2013 Jul 23;8(7):e69426. doi: 10.1371/journal.pone.0069426. PMID: 23936012; PMCID: PMC3720567.

Völgyi B, Kovács-Oller T, Atlasz T, Wilhelm M, Gábriel R. Gap junctional coupling in the vertebrate retina: variations on one theme? Prog Retin Eye Res. 2013 May;34:1-18. doi: 10.1016/j.preteyeres.2012.12.002. Epub 2013 Jan 8. PMID: 23313713.

Lakk M, Szabó B, Völgyi B, Gábriel R, Dénes V. Development-related splicing regulates pituitary adenylate cyclase-activating polypeptide (PACAP) receptors in the retina. Invest Ophthalmol Vis Sci. 2012 Nov 27;53(12):7825-32. doi: 10.1167/iovs.12-10417. PMID: 23099490.

Osterhout JA, Josten N, Yamada J, Pan F, Wu SW, Nguyen PL, Panagiotakos G, Inoue YU, Egusa SF, Volgyi B, Inoue T, Bloomfield SA, Barres BA, Berson DM, Feldheim DA, Huberman AD. Cadherin-6 mediates axon-target matching in a non- image-forming visual circuit. Neuron. 2011 Aug 25;71(4):632-9. doi: 10.1016/j.neuron.2011.07.006. PMID: 21867880; PMCID: PMC3513360.

Farajian R, Pan F, Akopian A, Völgyi B, Bloomfield SA. Masked excitatory crosstalk between the ON and OFF visual pathways in the mammalian retina. J Physiol. 2011 Sep 15;589(Pt 18):4473-89. doi: 10.1113/jphysiol.2011.213371. Epub 2011 Jul 18. PMID: 21768265; PMCID: PMC3208219.

Hu EH, Pan F, Völgyi B, Bloomfield SA. Light increases the gap junctional coupling of retinal ganglion cells. J Physiol. 2010 Nov 1;588(Pt 21):4145-63. doi: 10.1113/jphysiol.2010.193268. PMID: 20819943; PMCID: PMC3002447.

Pan F, Paul DL, Bloomfield SA, Völgyi B. Connexin36 is required for gap junctional coupling of most ganglion cell subtypes in the mouse retina. J Comp Neurol. 2010 Mar 15;518(6):911-27. doi: 10.1002/cne.22254. PMID: 20058323; PMCID: PMC2860380.

Retinal signalization team:

Gábriel R, Pöstyéni E, Dénes V. Neuroprotective Potential of Pituitary Adenylate Cyclase Activating Polypeptide in Retinal Degenerations of Metabolic Origin. Front Neurosci. 2019;13:1031. Published 2019 Oct 9. doi:10.3389/fnins.2019.01031

Kovacs K, Vaczy A, Fekete K, Kovari P, Atlasz T, Reglodi D, Gabriel R, Gallyas F, Sumegi B. PARP Inhibitor Protects Against Chronic Hypoxia/Reoxygenation-Induced Retinal Injury by Regulation of MAPKs, HIF1α, Nrf2, and NFκB. Invest Ophthalmol Vis Sci. 2019 Apr 1;60(5):1478-1490. doi: 10.1167/iovs.18-25936. PMID: 30973576.

Kovács-Valasek A, Szalontai B, Sétáló G Jr, Gábriel R. Sensitive fluorescent hybridisation protocol development for simultaneous detection of microRNA and cellular marker proteins (in the retina). Histochem Cell Biol. 2018 Nov;150(5):557-566. doi: 10.1007/s00418-018-1705-6. Epub 2018 Aug 7. PMID: 30088096; PMCID: PMC6182695.

Kovács-Valasek A, Szabadfi K, Dénes V, Szalontai B, Tamás A, Kiss P, Szabó A, Setalo G Jr, Reglődi D, Gábriel R. Accelerated retinal aging in PACAP knock-out mice. Neuroscience. 2017 Apr 21;348:1-10. doi: 10.1016/j.neuroscience.2017.02.003. Epub 2017 Feb 13. PMID: 28215987.

Lakk M, Denes V, Kovacs K, Hideg O, Szabo BF, Gabriel R. Pituitary Adenylate Cyclase-Activating Peptide (PACAP), a Novel Secretagogue, Regulates Secreted Morphogens in Newborn Rat Retina. Invest Ophthalmol Vis Sci. 2017 Jan 1;58(1):565-572. doi: 10.1167/iovs.16-20566. PMID: 28125843.

Hajna Z, Szabadfi K, Balla Z, Biró Z, Degrell P, Molnár GA, Kőszegi T, Tékus V, Helyes Z, Dobos A, Farkas S, Szűcs G, Gábriel R, Pintér E. Modeling long-term diabetes and related complications in rats. J Pharmacol Toxicol Methods. 2016 Mar-Apr;78:1-12. doi: 10.1016/j.vascn.2015.11.003. Epub 2015 Nov 14. PMID: 26589430.

Szabadfi K, Estrada C, Fernandez-Villalba E, Tarragon E, Setalo G Jr, Izura V, Reglodi D, Tamas A, Gabriel R, Herrero MT. Retinal aging in the diurnal Chilean rodent (Octodon degus): histological, ultrastructural and neurochemical alterations of the vertical information processing pathway. Front Cell Neurosci. 2015 Apr 21;9:126. doi: 10.3389/fncel.2015.00126. PMID: 25954153; PMCID: PMC4405622.

Yi F, Catudio-Garrett E, Gábriel R, Wilhelm M, Erdelyi F, Szabo G, Deisseroth K, Lawrence J. Hippocampal "cholinergic interneurons" visualized with the choline acetyltransferase promoter: anatomical distribution, intrinsic membrane properties, neurochemical characteristics, and capacity for cholinergic modulation. Front Synaptic Neurosci. 2015 Mar 6;7:4. doi: 10.3389/fnsyn.2015.00004. PMID: 25798106; PMCID: PMC4351620.

 

Dr. Róbert Gábriel: NKFIH119289, National Brain Project KTIA_NAP_13-A-I/12;

Dr. Völgyi Béla: OTKA K105247; National Excellence Program, Szent-Györgyi Albert Senior Researcher Fellowship TÁMOP-4.2.4.A/ 2-11/1-2012-0001; National Brain Project KTIA_NAP_13-2-2015-0008.

Kovács-Öller Tamás: Pécsi Tudományegyetem Tehetségcentruma Fiatal Kiválósága (2019); Szentágothai János Tehetségtámogató Program (2019-2022); PTE, Simonyi Innovációs Díj: CellZeus (2015); Apáczai Csere János Doktoranduszi Ösztöndíj (2013-2014, TÁMOP-4.2.4.A/ 2-11/1-2012-0001); IBRO, In Europe Short Stay Grant: Roska Botond labor, FMI, Basel, Svájc (2013 feb.)

  • Histological, molecular biological and light- and electronmicroscopical examination of transmitters and their receptors
  • Histological and molecular biological examination of apoptotic mechanisms
  • Imaging experiments (Ca++- imaging)
  • Extracellular electrophysiological recordings
  • Multielectrode extracellular recordings
  • Patch-clamp electrophysiological recordings
  • Molecular neurobiology laboratory (Western-blot, RT-PCR, qPCR)
  • Histology lab (microtomes for light- and electron-microscopy, dissecting microscopes, digital photomicroscope)
  • Electrophysiology lab (3 electrophysiology setups; amplifiers (patch-clamp, extracellular AC, multielectrode MEA, horizontal electrode puller, micromanipulators, ant-vibration table, analog-digital converters, signal synchronization module etc.)
  • Ca++- imaging laboratory (2 TILL photonics system setups, Polychrome 5 monochromator light stimulators, Retiga2000 CCD camera, Andor895 camera, Nikon CCD camera)

Retinal neurobiology research group

CONTACT
Dr. Béla Völgyi
Research Group Leader
 
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