Variations in the proliferative activity of the peripheral retina correlate with postnatal ocular growth in squamate reptiles

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Abstract

Abstract The retina is a complex, multilayered tissue responsible for the perception of visual stimuli from the environment. Contrary to mammals, the capacity for postnatal eye growth in fish and amphibians, and to a lower extent in birds, is coordinated with a progenitor population residing in the ciliary marginal zone (CMZ) at the retinal peripheral margin. However, little is known about embryonic retinogenesis and postnatal retinal growth in squamates (lizards, snakes), despite their exceptional array of ecologies and ocular morphologies. Here we address this gap by performing the first large-scale study assessing both ontogenetic and adult changes in the stem/progenitor activity of the squamate peripheral retina. Our study reveals for the first time that squamates exhibit a source of proliferating progenitors persisting post embryogenesis in a newly identified retinociliary junction anteriorly adjacent to the retina. This region is strikingly similar to the vertebrate CMZ by its peripheral location and pseudostratified nature, and shares a common pattern of slow-cycling cells, spatial differentiation gradient, and response to postnatal ocular growth. Additionally, its proliferative activity varies considerably among squamate species, in correlation with embryonic and postnatal differences in eye size and growth. Together our data indicate that squamates possess a proliferative peripheral retina that acts as a source of progenitors to compensate, at least in part, for postnatal ocular growth. Our findings also highlight the remarkable variation in activity and location of vertebrate retinal progenitors, indicating that the currently accepted scenario of reduced CMZ activity over the course of evolution is too simplistic. This article is protected by copyright. All rights reserved.
Original languageEnglish
JournalJournal of Comparative Neurology
ISSN0021-9967
DOIs
Publication statusE-pub ahead of print - 12 Mar 2019
MoE publication typeA1 Journal article-refereed

Fields of Science

  • squamates
  • peripheral retina
  • progenitors
  • ocular growth
  • evolution
  • development
  • RRID: SCR_007353
  • RRID: SCR_016299
  • RRID: AB_2734716
  • RRID: AB_305426
  • RRID: AB_305702
  • RRID: AB_561007
  • RRID: AB_1795608
  • RRID: AB_221448
  • RRID: AB_314691
  • RRID: AB_2341193
  • RRID: AB_2239761
  • RRID: AB_143165
  • RRID: AB_143157
  • RRID: SCR_014199
  • 1184 Genetics, developmental biology, physiology

Cite this

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title = "Variations in the proliferative activity of the peripheral retina correlate with postnatal ocular growth in squamate reptiles",
abstract = "Abstract The retina is a complex, multilayered tissue responsible for the perception of visual stimuli from the environment. Contrary to mammals, the capacity for postnatal eye growth in fish and amphibians, and to a lower extent in birds, is coordinated with a progenitor population residing in the ciliary marginal zone (CMZ) at the retinal peripheral margin. However, little is known about embryonic retinogenesis and postnatal retinal growth in squamates (lizards, snakes), despite their exceptional array of ecologies and ocular morphologies. Here we address this gap by performing the first large-scale study assessing both ontogenetic and adult changes in the stem/progenitor activity of the squamate peripheral retina. Our study reveals for the first time that squamates exhibit a source of proliferating progenitors persisting post embryogenesis in a newly identified retinociliary junction anteriorly adjacent to the retina. This region is strikingly similar to the vertebrate CMZ by its peripheral location and pseudostratified nature, and shares a common pattern of slow-cycling cells, spatial differentiation gradient, and response to postnatal ocular growth. Additionally, its proliferative activity varies considerably among squamate species, in correlation with embryonic and postnatal differences in eye size and growth. Together our data indicate that squamates possess a proliferative peripheral retina that acts as a source of progenitors to compensate, at least in part, for postnatal ocular growth. Our findings also highlight the remarkable variation in activity and location of vertebrate retinal progenitors, indicating that the currently accepted scenario of reduced CMZ activity over the course of evolution is too simplistic. This article is protected by copyright. All rights reserved.",
keywords = "squamates, peripheral retina, progenitors, ocular growth, evolution, development, RRID: SCR_007353, RRID: SCR_016299, RRID: AB_2734716, RRID: AB_305426, RRID: AB_305702, RRID: AB_561007, RRID: AB_1795608, RRID: AB_221448, RRID: AB_314691, RRID: AB_2341193, RRID: AB_2239761, RRID: AB_143165, RRID: AB_143157, RRID: SCR_014199, 1184 Genetics, developmental biology, physiology",
author = "Julia Eymann and Lotta Salomies and Simone Macr{\`i} and Nicolas Di-Po{\"i}",
year = "2019",
month = "3",
day = "12",
doi = "10.1002/cne.24677",
language = "English",
journal = "Journal of Comparative Neurology",
issn = "0021-9967",
publisher = "Wiley",

}

TY - JOUR

T1 - Variations in the proliferative activity of the peripheral retina correlate with postnatal ocular growth in squamate reptiles

AU - Eymann, Julia

AU - Salomies, Lotta

AU - Macrì, Simone

AU - Di-Poï, Nicolas

PY - 2019/3/12

Y1 - 2019/3/12

N2 - Abstract The retina is a complex, multilayered tissue responsible for the perception of visual stimuli from the environment. Contrary to mammals, the capacity for postnatal eye growth in fish and amphibians, and to a lower extent in birds, is coordinated with a progenitor population residing in the ciliary marginal zone (CMZ) at the retinal peripheral margin. However, little is known about embryonic retinogenesis and postnatal retinal growth in squamates (lizards, snakes), despite their exceptional array of ecologies and ocular morphologies. Here we address this gap by performing the first large-scale study assessing both ontogenetic and adult changes in the stem/progenitor activity of the squamate peripheral retina. Our study reveals for the first time that squamates exhibit a source of proliferating progenitors persisting post embryogenesis in a newly identified retinociliary junction anteriorly adjacent to the retina. This region is strikingly similar to the vertebrate CMZ by its peripheral location and pseudostratified nature, and shares a common pattern of slow-cycling cells, spatial differentiation gradient, and response to postnatal ocular growth. Additionally, its proliferative activity varies considerably among squamate species, in correlation with embryonic and postnatal differences in eye size and growth. Together our data indicate that squamates possess a proliferative peripheral retina that acts as a source of progenitors to compensate, at least in part, for postnatal ocular growth. Our findings also highlight the remarkable variation in activity and location of vertebrate retinal progenitors, indicating that the currently accepted scenario of reduced CMZ activity over the course of evolution is too simplistic. This article is protected by copyright. All rights reserved.

AB - Abstract The retina is a complex, multilayered tissue responsible for the perception of visual stimuli from the environment. Contrary to mammals, the capacity for postnatal eye growth in fish and amphibians, and to a lower extent in birds, is coordinated with a progenitor population residing in the ciliary marginal zone (CMZ) at the retinal peripheral margin. However, little is known about embryonic retinogenesis and postnatal retinal growth in squamates (lizards, snakes), despite their exceptional array of ecologies and ocular morphologies. Here we address this gap by performing the first large-scale study assessing both ontogenetic and adult changes in the stem/progenitor activity of the squamate peripheral retina. Our study reveals for the first time that squamates exhibit a source of proliferating progenitors persisting post embryogenesis in a newly identified retinociliary junction anteriorly adjacent to the retina. This region is strikingly similar to the vertebrate CMZ by its peripheral location and pseudostratified nature, and shares a common pattern of slow-cycling cells, spatial differentiation gradient, and response to postnatal ocular growth. Additionally, its proliferative activity varies considerably among squamate species, in correlation with embryonic and postnatal differences in eye size and growth. Together our data indicate that squamates possess a proliferative peripheral retina that acts as a source of progenitors to compensate, at least in part, for postnatal ocular growth. Our findings also highlight the remarkable variation in activity and location of vertebrate retinal progenitors, indicating that the currently accepted scenario of reduced CMZ activity over the course of evolution is too simplistic. This article is protected by copyright. All rights reserved.

KW - squamates

KW - peripheral retina

KW - progenitors

KW - ocular growth

KW - evolution

KW - development

KW - RRID: SCR_007353

KW - RRID: SCR_016299

KW - RRID: AB_2734716

KW - RRID: AB_305426

KW - RRID: AB_305702

KW - RRID: AB_561007

KW - RRID: AB_1795608

KW - RRID: AB_221448

KW - RRID: AB_314691

KW - RRID: AB_2341193

KW - RRID: AB_2239761

KW - RRID: AB_143165

KW - RRID: AB_143157

KW - RRID: SCR_014199

KW - 1184 Genetics, developmental biology, physiology

U2 - 10.1002/cne.24677

DO - 10.1002/cne.24677

M3 - Article

JO - Journal of Comparative Neurology

JF - Journal of Comparative Neurology

SN - 0021-9967

ER -