Sources and sink of retinoic acid in the embryonic chick retina

distribution of aldehyde dehydrogenase activities, CRABP-I, and sites of retinoic acid inactivation

Jorg Mey, Peter McCaffery, Monika Klemeit

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

Previous experiments in mice and zebrafish led to the hypothesis that an asymmetric distribution of the transcriptional activator retinoic acid (RA) causes ventral-dorsal polarity in the vertebrate eye anlage. A high concentration of RA in the ventral retinal neuroepithelium has been suggested to induce developmental events that finally establish topographic order in the retinotectal projection along the vertical eye axis. In the present study we have investigated potential sources and sinks of RA during embryonic development of the chick retina. At embryonic day (E)1 to E2, when the spatial determination of the eye primordia takes place, no RA synthesis by aldehyde dehydrogenases was detectable, and neither immunoreactivity for retinaldehyde dehydrogenase RALDH-2 nor for cellular retinoic acid binding protein CRABP-I was observed. These components of RA signal transduction appeared in the eye between E3 and E5. At later stages, RA-measurements with a reporter cell line showed highest synthesis in the retinal pigment epithelium (RPE) and at the ventral and dorsal poles of the retina. RA degradation occurred mostly in a horizontal region in the middle of the retina with only small differences along the nasal-temporal axis. CRABP-I immunoreactivity appeared first in differentiating retinal ganglion cells with no indication of a spatial gradient across the ventral-dorsal eye axis. RA-production depended on three NAD+-dependent enzyme activities, which could be competitively inhibited by citral. One enzyme, located in the dorsal retina (corresponding to mouse RALDH-1), and one enzyme in the RPE (RALDH-2) were aldehyde dehydrogenases of the same molecular weight (monomers about 55 kDa) but with different isoelectric points (6.5-6.9; 4.9-5.4). The third RA-synthesizing activity (pI 6.0-6.3) was limited to the ventral retina, and likely corresponded to mouse RALDH-3. The restricted localization of retinoid-metabolizing activities along the dorsal-ventral axis of the embryonic chick retina does support the idea that RA is involved in dorsal-ventral eye patterning. However, the late time of appearance of aldehyde dehydrogenase activities and CRABP-I points to functions in cellular differentiation that are distinct from the initiation of the dorsal-ventral polarity.
Original languageEnglish
Pages (from-to)135-148
Number of pages14
JournalDevelopmental Brain Research
Volume127
Issue number2
Early online date6 Feb 2001
DOIs
Publication statusPublished - 30 Apr 2001

Keywords

  • aldehyde dehydrogenase
  • animals
  • cell differentiation
  • cell polarity
  • chick embryo
  • immunohistochemistry
  • receptors, retinoic acid
  • retina
  • retinal ganglion cells
  • tretinoin
  • chick development
  • retinoic acid
  • CRABP
  • axial polarity
  • binding-protein
  • retinaldehyde dehydrogenase
  • synthesizing enzyme
  • mouse development
  • ventral retina
  • spinal-cord
  • expression
  • differentiation
  • photoreceptors
  • identification
  • development and regeneration
  • pattern formation
  • compartments
  • boundaries

Cite this

@article{73120c6cc7254876a3b51058aff5b5eb,
title = "Sources and sink of retinoic acid in the embryonic chick retina: distribution of aldehyde dehydrogenase activities, CRABP-I, and sites of retinoic acid inactivation",
abstract = "Previous experiments in mice and zebrafish led to the hypothesis that an asymmetric distribution of the transcriptional activator retinoic acid (RA) causes ventral-dorsal polarity in the vertebrate eye anlage. A high concentration of RA in the ventral retinal neuroepithelium has been suggested to induce developmental events that finally establish topographic order in the retinotectal projection along the vertical eye axis. In the present study we have investigated potential sources and sinks of RA during embryonic development of the chick retina. At embryonic day (E)1 to E2, when the spatial determination of the eye primordia takes place, no RA synthesis by aldehyde dehydrogenases was detectable, and neither immunoreactivity for retinaldehyde dehydrogenase RALDH-2 nor for cellular retinoic acid binding protein CRABP-I was observed. These components of RA signal transduction appeared in the eye between E3 and E5. At later stages, RA-measurements with a reporter cell line showed highest synthesis in the retinal pigment epithelium (RPE) and at the ventral and dorsal poles of the retina. RA degradation occurred mostly in a horizontal region in the middle of the retina with only small differences along the nasal-temporal axis. CRABP-I immunoreactivity appeared first in differentiating retinal ganglion cells with no indication of a spatial gradient across the ventral-dorsal eye axis. RA-production depended on three NAD+-dependent enzyme activities, which could be competitively inhibited by citral. One enzyme, located in the dorsal retina (corresponding to mouse RALDH-1), and one enzyme in the RPE (RALDH-2) were aldehyde dehydrogenases of the same molecular weight (monomers about 55 kDa) but with different isoelectric points (6.5-6.9; 4.9-5.4). The third RA-synthesizing activity (pI 6.0-6.3) was limited to the ventral retina, and likely corresponded to mouse RALDH-3. The restricted localization of retinoid-metabolizing activities along the dorsal-ventral axis of the embryonic chick retina does support the idea that RA is involved in dorsal-ventral eye patterning. However, the late time of appearance of aldehyde dehydrogenase activities and CRABP-I points to functions in cellular differentiation that are distinct from the initiation of the dorsal-ventral polarity.",
keywords = "aldehyde dehydrogenase, animals, cell differentiation, cell polarity, chick embryo, immunohistochemistry, receptors, retinoic acid, retina, retinal ganglion cells, tretinoin, chick development, retinoic acid, CRABP, axial polarity, binding-protein, retinaldehyde dehydrogenase, synthesizing enzyme, mouse development, ventral retina, spinal-cord, expression, differentiation, photoreceptors, identification, development and regeneration, pattern formation, compartments, boundaries",
author = "Jorg Mey and Peter McCaffery and Monika Klemeit",
year = "2001",
month = "4",
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doi = "10.1016/S0165-3806(01)00127-4",
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volume = "127",
pages = "135--148",
journal = "Developmental Brain Research",
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TY - JOUR

T1 - Sources and sink of retinoic acid in the embryonic chick retina

T2 - distribution of aldehyde dehydrogenase activities, CRABP-I, and sites of retinoic acid inactivation

AU - Mey, Jorg

AU - McCaffery, Peter

AU - Klemeit, Monika

PY - 2001/4/30

Y1 - 2001/4/30

N2 - Previous experiments in mice and zebrafish led to the hypothesis that an asymmetric distribution of the transcriptional activator retinoic acid (RA) causes ventral-dorsal polarity in the vertebrate eye anlage. A high concentration of RA in the ventral retinal neuroepithelium has been suggested to induce developmental events that finally establish topographic order in the retinotectal projection along the vertical eye axis. In the present study we have investigated potential sources and sinks of RA during embryonic development of the chick retina. At embryonic day (E)1 to E2, when the spatial determination of the eye primordia takes place, no RA synthesis by aldehyde dehydrogenases was detectable, and neither immunoreactivity for retinaldehyde dehydrogenase RALDH-2 nor for cellular retinoic acid binding protein CRABP-I was observed. These components of RA signal transduction appeared in the eye between E3 and E5. At later stages, RA-measurements with a reporter cell line showed highest synthesis in the retinal pigment epithelium (RPE) and at the ventral and dorsal poles of the retina. RA degradation occurred mostly in a horizontal region in the middle of the retina with only small differences along the nasal-temporal axis. CRABP-I immunoreactivity appeared first in differentiating retinal ganglion cells with no indication of a spatial gradient across the ventral-dorsal eye axis. RA-production depended on three NAD+-dependent enzyme activities, which could be competitively inhibited by citral. One enzyme, located in the dorsal retina (corresponding to mouse RALDH-1), and one enzyme in the RPE (RALDH-2) were aldehyde dehydrogenases of the same molecular weight (monomers about 55 kDa) but with different isoelectric points (6.5-6.9; 4.9-5.4). The third RA-synthesizing activity (pI 6.0-6.3) was limited to the ventral retina, and likely corresponded to mouse RALDH-3. The restricted localization of retinoid-metabolizing activities along the dorsal-ventral axis of the embryonic chick retina does support the idea that RA is involved in dorsal-ventral eye patterning. However, the late time of appearance of aldehyde dehydrogenase activities and CRABP-I points to functions in cellular differentiation that are distinct from the initiation of the dorsal-ventral polarity.

AB - Previous experiments in mice and zebrafish led to the hypothesis that an asymmetric distribution of the transcriptional activator retinoic acid (RA) causes ventral-dorsal polarity in the vertebrate eye anlage. A high concentration of RA in the ventral retinal neuroepithelium has been suggested to induce developmental events that finally establish topographic order in the retinotectal projection along the vertical eye axis. In the present study we have investigated potential sources and sinks of RA during embryonic development of the chick retina. At embryonic day (E)1 to E2, when the spatial determination of the eye primordia takes place, no RA synthesis by aldehyde dehydrogenases was detectable, and neither immunoreactivity for retinaldehyde dehydrogenase RALDH-2 nor for cellular retinoic acid binding protein CRABP-I was observed. These components of RA signal transduction appeared in the eye between E3 and E5. At later stages, RA-measurements with a reporter cell line showed highest synthesis in the retinal pigment epithelium (RPE) and at the ventral and dorsal poles of the retina. RA degradation occurred mostly in a horizontal region in the middle of the retina with only small differences along the nasal-temporal axis. CRABP-I immunoreactivity appeared first in differentiating retinal ganglion cells with no indication of a spatial gradient across the ventral-dorsal eye axis. RA-production depended on three NAD+-dependent enzyme activities, which could be competitively inhibited by citral. One enzyme, located in the dorsal retina (corresponding to mouse RALDH-1), and one enzyme in the RPE (RALDH-2) were aldehyde dehydrogenases of the same molecular weight (monomers about 55 kDa) but with different isoelectric points (6.5-6.9; 4.9-5.4). The third RA-synthesizing activity (pI 6.0-6.3) was limited to the ventral retina, and likely corresponded to mouse RALDH-3. The restricted localization of retinoid-metabolizing activities along the dorsal-ventral axis of the embryonic chick retina does support the idea that RA is involved in dorsal-ventral eye patterning. However, the late time of appearance of aldehyde dehydrogenase activities and CRABP-I points to functions in cellular differentiation that are distinct from the initiation of the dorsal-ventral polarity.

KW - aldehyde dehydrogenase

KW - animals

KW - cell differentiation

KW - cell polarity

KW - chick embryo

KW - immunohistochemistry

KW - receptors, retinoic acid

KW - retina

KW - retinal ganglion cells

KW - tretinoin

KW - chick development

KW - retinoic acid

KW - CRABP

KW - axial polarity

KW - binding-protein

KW - retinaldehyde dehydrogenase

KW - synthesizing enzyme

KW - mouse development

KW - ventral retina

KW - spinal-cord

KW - expression

KW - differentiation

KW - photoreceptors

KW - identification

KW - development and regeneration

KW - pattern formation

KW - compartments

KW - boundaries

U2 - 10.1016/S0165-3806(01)00127-4

DO - 10.1016/S0165-3806(01)00127-4

M3 - Article

VL - 127

SP - 135

EP - 148

JO - Developmental Brain Research

JF - Developmental Brain Research

SN - 0165-3806

IS - 2

ER -