Spatial Expression Pattern of the Major Ca-Buffer Proteins in Mouse Retinal Ganglion Cells

Overview

Journal Cells

Publisher MDPI

Specialties Biochemistry
Biophysics
Cell Biology
Molecular Biology

Date 2020 Mar 29

PMID 32218175

Citations 9

Authors

Tamas Kovacs-Oller

Gergely Szarka

Adam J Tengolics

Alma Ganczer

Boglarka Balogh

Edina Szabo-Meleg

Miklos Nyitrai

Bela Volgyi

Affiliations

Soon will be listed here.

Abstract

The most prevalent Ca-buffer proteins (CaBPs: parvalbumin-PV; calbindin-CaB; calretinin-CaR) are widely expressed by various neurons throughout the brain, including the retinal ganglion cells (RGCs). Even though their retinal expression has been extensively studied, a coherent assessment of topographical variations is missing. To examine this, we performed immunohistochemistry (IHC) in mouse retinas. We found variability in the expression levels and cell numbers for CaR, with stronger and more numerous labels in the dorso-central area. CaBP+ cells contributed to RGCs with all soma sizes, indicating heterogeneity. We separated four to nine RGC clusters in each area based on expression levels and soma sizes. Besides the overall high variety in cluster number and size, the peripheral half of the temporal retina showed the greatest cluster number, indicating a better separation of RGC subtypes there. Multiple labels showed that 39% of the RGCs showed positivity for a single CaBP, 30% expressed two CaBPs, 25% showed no CaBP expression, and 6% expressed all three proteins. Finally, we observed an inverse relation between CaB and CaR expression levels in CaB/CaR dual- and CaB/CaR/PV triple-labeled RGCs, suggesting a mutual complementary function.

Citing Articles

Deletion of myeloid HDAC3 promotes efferocytosis to ameliorate retinal ischemic injury.

Shahror R, Shosha E, Morris C, Wild M, Mu S, Csanyi G J Neuroinflammation. 2024; 21(1):170.

PMID: 38997746 PMC: 11241909. DOI: 10.1186/s12974-024-03159-8.

The RBPMS mouse line for studying retinal and vascular relevant diseases.

Li G, Luo Y, Zhang Q, Chen W, Lai K, Liu Y iScience. 2023; 26(11):108111.

PMID: 37867934 PMC: 10589894. DOI: 10.1016/j.isci.2023.108111.

Calbindin 2-specific deletion of arginase 2 preserves visual function after optic nerve crush.

Zaidi S, Xu Z, Lemtalsi T, Sandow P, Athota S, Liu F Cell Death Dis. 2023; 14(10):661.

PMID: 37816735 PMC: 10564748. DOI: 10.1038/s41419-023-06180-6.

Traumatic Brain Injury Induces Microglial and Caspase3 Activation in the Retina.

Kovacs-Oller T, Zempleni R, Balogh B, Szarka G, Fazekas B, Tengolics A Int J Mol Sci. 2023; 24(5).

PMID: 36901880 PMC: 10003323. DOI: 10.3390/ijms24054451.

A novel approach to the functional classification of retinal ganglion cells.

Hilgen G, Kartsaki E, Kartysh V, Cessac B, Sernagor E Open Biol. 2022; 12(3):210367.

PMID: 35259949 PMC: 8905177. DOI: 10.1098/rsob.210367.

References

Gabriel R, LeSauter J, Banvolgyi T, Petrovics G, Silver R, Witkovsky P . AII amacrine neurons of the rat retina show diurnal and circadian rhythms of parvalbumin immunoreactivity. Cell Tissue Res. 2003; 315(2):181-6. PMC: 3271844. DOI: 10.1007/s00441-003-0785-2. View

Kim T, Jeon C . Morphological classification of parvalbumin-containing retinal ganglion cells in mouse: single-cell injection after immunocytochemistry. Invest Ophthalmol Vis Sci. 2006; 47(7):2757-64. DOI: 10.1167/iovs.05-1442. View

Kovacs-Oller T, Debertin G, Balogh M, Ganczer A, Orban J, Nyitrai M . Connexin36 Expression in the Mammalian Retina: A Multiple-Species Comparison. Front Cell Neurosci. 2017; 11:65. PMC: 5343066. DOI: 10.3389/fncel.2017.00065. View

Rodriguez A, Perez de Sevilla Muller L, Brecha N . The RNA binding protein RBPMS is a selective marker of ganglion cells in the mammalian retina. J Comp Neurol. 2013; 522(6):1411-43. PMC: 3959221. DOI: 10.1002/cne.23521. View

Lee E, Kim T, Jeon C . Identification of parvalbumin-containing retinal ganglion cells in rabbit. Exp Eye Res. 2013; 110:113-24. DOI: 10.1016/j.exer.2013.02.018. View

Volgyi B, Abrams J, Paul D, Bloomfield S . Morphology and tracer coupling pattern of alpha ganglion cells in the mouse retina. J Comp Neurol. 2005; 492(1):66-77. PMC: 2834591. DOI: 10.1002/cne.20700. View

Noble J, Almalki R, Roe S, Wagner A, Duman R, Atack J . The X-ray structure of human calbindin-D28K: an improved model. Acta Crystallogr D Struct Biol. 2018; 74(Pt 10):1008-1014. PMC: 6173056. DOI: 10.1107/S2059798318011610. View

Volgyi B, Chheda S, Bloomfield S . Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. J Comp Neurol. 2008; 512(5):664-87. PMC: 3373319. DOI: 10.1002/cne.21912. View

Kovacs-Oller T, Szarka G, Ganczer A, Tengolics A, Balogh B, Volgyi B . Expression of Ca-Binding Buffer Proteins in the Human and Mouse Retinal Neurons. Int J Mol Sci. 2019; 20(9). PMC: 6539911. DOI: 10.3390/ijms20092229. View

10.

Lee E, Lee J, Kim G, Jeon C . Identification of calretinin-expressing retinal ganglion cells projecting to the mouse superior colliculus. Cell Tissue Res. 2018; 376(2):153-163. DOI: 10.1007/s00441-018-2964-1. View

11.

Tengolics A, Szarka G, Ganczer A, Szabo-Meleg E, Nyitrai M, Kovacs-Oller T . Response Latency Tuning by Retinal Circuits Modulates Signal Efficiency. Sci Rep. 2019; 9(1):15110. PMC: 6806000. DOI: 10.1038/s41598-019-51756-y. View

12.

Wei W, Elstrott J, Feller M . Two-photon targeted recording of GFP-expressing neurons for light responses and live-cell imaging in the mouse retina. Nat Protoc. 2010; 5(7):1347-52. PMC: 4303237. DOI: 10.1038/nprot.2010.106. View

13.

Schwaller B . The continuing disappearance of "pure" Ca2+ buffers. Cell Mol Life Sci. 2008; 66(2):275-300. PMC: 11131537. DOI: 10.1007/s00018-008-8564-6. View

14.

Kantor O, Mezey S, Adeghate J, Naumann A, Nitschke R, Enzsoly A . Calcium buffer proteins are specific markers of human retinal neurons. Cell Tissue Res. 2016; 365(1):29-50. DOI: 10.1007/s00441-016-2376-z. View

15.

Schubert T, Degen J, Willecke K, Hormuzdi S, Monyer H, Weiler R . Connexin36 mediates gap junctional coupling of alpha-ganglion cells in mouse retina. J Comp Neurol. 2005; 485(3):191-201. DOI: 10.1002/cne.20510. View

16.

Roy K, Kumar S, Bloomfield S . Gap junctional coupling between retinal amacrine and ganglion cells underlies coherent activity integral to global object perception. Proc Natl Acad Sci U S A. 2017; 114(48):E10484-E10493. PMC: 5715748. DOI: 10.1073/pnas.1708261114. View

17.

Stadler F, Schmutz I, Schwaller B, Albrecht U . Lack of calbindin-D28k alters response of the murine circadian clock to light. Chronobiol Int. 2010; 27(1):68-82. DOI: 10.3109/07420521003648554. View

18.

Schwaller B . Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol. 2010; 2(11):a004051. PMC: 2964180. DOI: 10.1101/cshperspect.a004051. View

19.

El-Danaf R, Huberman A . Sub-topographic maps for regionally enhanced analysis of visual space in the mouse retina. J Comp Neurol. 2018; 527(1):259-269. PMC: 6506235. DOI: 10.1002/cne.24457. View

20.

Volgyi B, Pollak E, Buzas P, Gabriel R . Calretinin in neurochemically well-defined cell populations of rabbit retina. Brain Res. 1997; 763(1):79-86. DOI: 10.1016/s0006-8993(97)00405-8. View