Anolis carolinensis as a model to understand the molecular and cellular basis of foveal development

Naif S. Sannan, Xianghong Shan, Kevin Gregory-Evans, Kenro Kusumi, Cheryl Y. Gregory-Evans

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

The fovea is an anatomical specialization of the central retina containing closely packed cone-photoreceptors providing an area of high acuity vision in humans and primates. Despite its key role in the clarity of vision, little is known about the molecular and cellular basis of foveal development, due to the absence of a foveal structure in commonly used laboratory animal models. Of the amniotes the retina in birds of prey and some reptiles do exhibit a typical foveal structure, but they have not been studied in the context of foveal development due to lack of availability of embryonic tissue, lack of captive breeding programs, and limited genomic information. However, the genome for the diurnal bifoveate reptile species Anolis carolinensis (green anole) was recently published and it is possible to collect embryos from this species in captivity. Here, we tested the feasibility of using the anole as a model to study foveal development. Eyes were collected at various stages of development for histological analysis, immunofluorescence, and apoptosis. We show that at embryonic stage (ES) 10 there is peak ganglion cell density at the incipient central foveal region and a single row of cone photoreceptor nuclei. At ES17 the foveal pit begins to form and at this stage there are 3–4 rows of cone nuclei. Post-hatching a further increase in cone density and lengthening of inner and outer segments is observed. A yellowish pigment was seen in the adult central foveal region, but not in the temporal fovea. At ES14 Pax6 was localized across the entire retina, but was more prominent in the ganglion cell layer (GCL) and the part of the inner nuclear layer (INL) containing amacrine cell bodies. However, at ES17 Pax6 expression in the ganglion cells of the central retina was markedly reduced. Bioinformatic analysis revealed that 86% of human candidate foveal hypoplasia genes had an orthologous gene or DNA sequence in the green anole. These findings provide the first insight into foveal morphogenesis in the green anole and suggest that it could be a very useful model for investigating the molecular signals driving foveal development, and thus inform on human foveal development and disease.

Original languageEnglish (US)
Pages (from-to)138-147
Number of pages10
JournalExperimental Eye Research
Volume173
DOIs
StatePublished - Aug 1 2018

Fingerprint

Retina
Ganglia
Retinal Cone Photoreceptor Cells
Reptiles
Raptors
Amacrine Cells
Molecular Models
Human Development
Computational Biology
Morphogenesis
Primates
Genes
Breeding
Fluorescent Antibody Technique
Embryonic Structures
Animal Models
Cell Count
Genome
Apoptosis

Keywords

  • Animal model
  • Anolis carolinensis
  • Development
  • Fovea
  • Green anole
  • Pax6

ASJC Scopus subject areas

  • Ophthalmology
  • Sensory Systems
  • Cellular and Molecular Neuroscience

Cite this

Anolis carolinensis as a model to understand the molecular and cellular basis of foveal development. / Sannan, Naif S.; Shan, Xianghong; Gregory-Evans, Kevin; Kusumi, Kenro; Gregory-Evans, Cheryl Y.

In: Experimental Eye Research, Vol. 173, 01.08.2018, p. 138-147.

Research output: Contribution to journalArticle

Sannan, Naif S. ; Shan, Xianghong ; Gregory-Evans, Kevin ; Kusumi, Kenro ; Gregory-Evans, Cheryl Y. / Anolis carolinensis as a model to understand the molecular and cellular basis of foveal development. In: Experimental Eye Research. 2018 ; Vol. 173. pp. 138-147.
@article{f3d77c114cc5490f8bf73087382d0923,
title = "Anolis carolinensis as a model to understand the molecular and cellular basis of foveal development",
abstract = "The fovea is an anatomical specialization of the central retina containing closely packed cone-photoreceptors providing an area of high acuity vision in humans and primates. Despite its key role in the clarity of vision, little is known about the molecular and cellular basis of foveal development, due to the absence of a foveal structure in commonly used laboratory animal models. Of the amniotes the retina in birds of prey and some reptiles do exhibit a typical foveal structure, but they have not been studied in the context of foveal development due to lack of availability of embryonic tissue, lack of captive breeding programs, and limited genomic information. However, the genome for the diurnal bifoveate reptile species Anolis carolinensis (green anole) was recently published and it is possible to collect embryos from this species in captivity. Here, we tested the feasibility of using the anole as a model to study foveal development. Eyes were collected at various stages of development for histological analysis, immunofluorescence, and apoptosis. We show that at embryonic stage (ES) 10 there is peak ganglion cell density at the incipient central foveal region and a single row of cone photoreceptor nuclei. At ES17 the foveal pit begins to form and at this stage there are 3–4 rows of cone nuclei. Post-hatching a further increase in cone density and lengthening of inner and outer segments is observed. A yellowish pigment was seen in the adult central foveal region, but not in the temporal fovea. At ES14 Pax6 was localized across the entire retina, but was more prominent in the ganglion cell layer (GCL) and the part of the inner nuclear layer (INL) containing amacrine cell bodies. However, at ES17 Pax6 expression in the ganglion cells of the central retina was markedly reduced. Bioinformatic analysis revealed that 86{\%} of human candidate foveal hypoplasia genes had an orthologous gene or DNA sequence in the green anole. These findings provide the first insight into foveal morphogenesis in the green anole and suggest that it could be a very useful model for investigating the molecular signals driving foveal development, and thus inform on human foveal development and disease.",
keywords = "Animal model, Anolis carolinensis, Development, Fovea, Green anole, Pax6",
author = "Sannan, {Naif S.} and Xianghong Shan and Kevin Gregory-Evans and Kenro Kusumi and Gregory-Evans, {Cheryl Y.}",
year = "2018",
month = "8",
day = "1",
doi = "10.1016/j.exer.2018.05.012",
language = "English (US)",
volume = "173",
pages = "138--147",
journal = "Experimental Eye Research",
issn = "0014-4835",
publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Anolis carolinensis as a model to understand the molecular and cellular basis of foveal development

AU - Sannan, Naif S.

AU - Shan, Xianghong

AU - Gregory-Evans, Kevin

AU - Kusumi, Kenro

AU - Gregory-Evans, Cheryl Y.

PY - 2018/8/1

Y1 - 2018/8/1

N2 - The fovea is an anatomical specialization of the central retina containing closely packed cone-photoreceptors providing an area of high acuity vision in humans and primates. Despite its key role in the clarity of vision, little is known about the molecular and cellular basis of foveal development, due to the absence of a foveal structure in commonly used laboratory animal models. Of the amniotes the retina in birds of prey and some reptiles do exhibit a typical foveal structure, but they have not been studied in the context of foveal development due to lack of availability of embryonic tissue, lack of captive breeding programs, and limited genomic information. However, the genome for the diurnal bifoveate reptile species Anolis carolinensis (green anole) was recently published and it is possible to collect embryos from this species in captivity. Here, we tested the feasibility of using the anole as a model to study foveal development. Eyes were collected at various stages of development for histological analysis, immunofluorescence, and apoptosis. We show that at embryonic stage (ES) 10 there is peak ganglion cell density at the incipient central foveal region and a single row of cone photoreceptor nuclei. At ES17 the foveal pit begins to form and at this stage there are 3–4 rows of cone nuclei. Post-hatching a further increase in cone density and lengthening of inner and outer segments is observed. A yellowish pigment was seen in the adult central foveal region, but not in the temporal fovea. At ES14 Pax6 was localized across the entire retina, but was more prominent in the ganglion cell layer (GCL) and the part of the inner nuclear layer (INL) containing amacrine cell bodies. However, at ES17 Pax6 expression in the ganglion cells of the central retina was markedly reduced. Bioinformatic analysis revealed that 86% of human candidate foveal hypoplasia genes had an orthologous gene or DNA sequence in the green anole. These findings provide the first insight into foveal morphogenesis in the green anole and suggest that it could be a very useful model for investigating the molecular signals driving foveal development, and thus inform on human foveal development and disease.

AB - The fovea is an anatomical specialization of the central retina containing closely packed cone-photoreceptors providing an area of high acuity vision in humans and primates. Despite its key role in the clarity of vision, little is known about the molecular and cellular basis of foveal development, due to the absence of a foveal structure in commonly used laboratory animal models. Of the amniotes the retina in birds of prey and some reptiles do exhibit a typical foveal structure, but they have not been studied in the context of foveal development due to lack of availability of embryonic tissue, lack of captive breeding programs, and limited genomic information. However, the genome for the diurnal bifoveate reptile species Anolis carolinensis (green anole) was recently published and it is possible to collect embryos from this species in captivity. Here, we tested the feasibility of using the anole as a model to study foveal development. Eyes were collected at various stages of development for histological analysis, immunofluorescence, and apoptosis. We show that at embryonic stage (ES) 10 there is peak ganglion cell density at the incipient central foveal region and a single row of cone photoreceptor nuclei. At ES17 the foveal pit begins to form and at this stage there are 3–4 rows of cone nuclei. Post-hatching a further increase in cone density and lengthening of inner and outer segments is observed. A yellowish pigment was seen in the adult central foveal region, but not in the temporal fovea. At ES14 Pax6 was localized across the entire retina, but was more prominent in the ganglion cell layer (GCL) and the part of the inner nuclear layer (INL) containing amacrine cell bodies. However, at ES17 Pax6 expression in the ganglion cells of the central retina was markedly reduced. Bioinformatic analysis revealed that 86% of human candidate foveal hypoplasia genes had an orthologous gene or DNA sequence in the green anole. These findings provide the first insight into foveal morphogenesis in the green anole and suggest that it could be a very useful model for investigating the molecular signals driving foveal development, and thus inform on human foveal development and disease.

KW - Animal model

KW - Anolis carolinensis

KW - Development

KW - Fovea

KW - Green anole

KW - Pax6

UR - http://www.scopus.com/inward/record.url?scp=85047102173&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85047102173&partnerID=8YFLogxK

U2 - 10.1016/j.exer.2018.05.012

DO - 10.1016/j.exer.2018.05.012

M3 - Article

C2 - 29775563

AN - SCOPUS:85047102173

VL - 173

SP - 138

EP - 147

JO - Experimental Eye Research

JF - Experimental Eye Research

SN - 0014-4835

ER -