Acquisition of Retinoic Acid Signaling Pathway and Innovation of the Chordate Body Plan

Fujiwara, Shigeki; Kawamura, Kazuo

doi:10.2108/zsj.20.809

Cited by 41 publications

(34 citation statements)

References 122 publications

(95 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The acquisition of the anterioposterior organized body plan in chordates coincides with the innovation of RA and its nuclear receptor to control development. No retinoic acid receptors have so far been found in nonchordate species (52). Identification of a putative ascidian RetSat underscores the potential importance of the pathway that starts with the saturation of the 13-14 double bond of retinol.…”

Section: Discussionmentioning

confidence: 98%

Identification of All-trans-Retinol:All-trans-13,14-dihydroretinol Saturase

Moise¹,

Kuksa²,

Imanishi³

et al. 2004

Journal of Biological Chemistry

117

View full text Add to dashboard Cite

Retinoids carry out essential functions in vertebrate development and vision. Many of the retinoid processing enzymes remain to be identified at the molecular level. To expand the knowledge of retinoid biochemistry in vertebrates, we studied the enzymes involved in plant metabolism of carotenoids, a related group of compounds. We identified a family of vertebrate enzymes that share significant similarity and a putative phytoene desaturase domain with a recently described plant carotenoid isomerase (CRTISO), which isomerizes prolycopene to all-trans-lycopene. Comparison of heterologously expressed mouse and plant enzymes indicates that unlike plant CRTISO, the CRTISO-related mouse enzyme is inactive toward prolycopene. Instead, the CRTISO-related mouse enzyme is a retinol saturase carrying out the saturation of the 13-14 double bond of all-trans-retinol to produce all-trans-13,14-dihydroretinol. The product of mouse retinol saturase (RetSat) has a shifted UV absorbance maximum, max ‫؍‬ 290 nm, compared with the parent compound, all-trans-retinol ( max ‫؍‬ 325 nm), and its MS analysis (m/z ‫؍‬ 288) indicates saturation of a double bond. The product was further identified as all-trans-13,14-dihydroretinol, since its characteristics were identical to those of a synthetic standard. Mouse RetSat is membrane-associated and expressed in many tissues, with the highest levels in liver, kidney, and intestine. All-trans-13,14-dihydroretinol was also detected in several tissues of animals maintained on a normal diet. Thus, saturation of all-transretinol to all-trans-13,14-dihydroretinol by RetSat produces a new metabolite of yet unknown biological function.Retinoids are essential for many important biological functions, such as development, immunity, cellular differentiation, and vision of vertebrates. Retinoids encompassing both natural derivatives of all-trans-retinol and their synthetic analogues exert their functions through several active compounds. Esterification of retinol by lecithin-retinol acyltransferase (LRAT)

show abstract

Section: Discussionmentioning

confidence: 98%

Identification of All-trans-Retinol:All-trans-13,14-dihydroretinol Saturase

Moise¹,

Kuksa²,

Imanishi³

et al. 2004

Journal of Biological Chemistry

117

View full text Add to dashboard Cite

show abstract

“…In C. intestinalis, ALDH1a is expressed in a sharp, posterior mesodermal domain in the early embryo (at 5-8 h) (Fig. S4) (30). At later embryonic stages, ALDH1a is detectable in a distinct domain in the posterior gut endoderm of the amphioxus late embryo (at 24 h) and in the posterior trunk of C. intestinalis (at 10-12 h).…”

Section: Invertebrate Chordate Aldh1 Channel Switch Is Associated Withmentioning

confidence: 91%

Structural shifts of aldehyde dehydrogenase enzymes were instrumental for the early evolution of retinoid-dependent axial patterning in metazoans

Sobreira

Marlétaz²,

Simões-Costa³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Aldehyde dehydrogenases (ALDHs) catabolize toxic aldehydes and process the vitamin A-derived retinaldehyde into retinoic acid (RA), a small diffusible molecule and a pivotal chordate morphogen. In this study, we combine phylogenetic, structural, genomic, and developmental gene expression analyses to examine the evolutionary origins of ALDH substrate preference. Structural modeling reveals that processing of small aldehydes, such as acetaldehyde, by ALDH2, versus large aldehydes, including retinaldehyde, by ALDH1A is associated with small versus large substrate entry channels (SECs), respectively. Moreover, we show that metazoan ALDH1s and ALDH2s are members of a single ALDH1/2 clade and that during evolution, eukaryote ALDH1/2s often switched between large and small SECs after gene duplication, transforming constricted channels into wide opened ones and vice versa. Ancestral sequence reconstructions suggest that during the evolutionary emergence of RA signaling, the ancestral, narrow-channeled metazoan ALDH1/2 gave rise to large ALDH1 channels capable of accommodating bulky aldehydes, such as retinaldehyde, supporting the view that retinoid-dependent signaling arose from ancestral cellular detoxification mechanisms. Our analyses also indicate that, on a more restricted evolutionary scale, ALDH1 duplicates from invertebrate chordates (amphioxus and ascidian tunicates) underwent switches to smaller and narrower SECs. When combined with alterations in gene expression, these switches led to neofunctionalization from ALDH1-like roles in embryonic patterning to systemic, ALDH2-like roles, suggesting functional shifts from signaling to detoxification.Aldehyde dehydrogenase phylogeny | Branchiostoma floridae | Ciona intestinalis versus Ciona savignyi | evolution of retinoic acid signaling | origins of morphogen-dependent signaling I n animal development, major signaling pathways are controlled by morphogens, diffusible molecules whose evolutionary origins are difficult to assess. Aldehyde dehydrogenase (ALDH) enzymes are attractive subjects to study the evolution of morphogen signaling for two main reasons. First, in addition to their acknowledged role in protecting animals by catabolizing reactive biogenic and xenobiotic aldehydes, some ALDHs also synthesize signaling molecules (1-3). Prime examples for these two ALDH enzyme roles are the ALDH2s, which degrade small toxic aldehydes, such as the acetaldehyde derived from ethanol metabolism (1, 2), and the ALDH1s, which process larger aldehydes, including retinaldehyde, a vitamin A-derived precursor of the morphogen retinoic acid (RA). RA plays a critical role during embryonic development of chordates (i.e., amphioxus, tunicates, and vertebrates) and has been suggested to have already been involved in patterning the last common ancestor of bilaterian animals (4-8).Second, ALDHs are among the best-characterized proteins, and their structure and substrate profiles have been determined with exquisite precision (9-15). Thus, structural modeling of these proteins can be used ...

show abstract

“…With more than 3000 species, Cypriniformes is the most diverse order of freshwater fishes with an impressive diversity in pharyngeal dentition [3]. Retinoic acid (RA) is a morphogen molecule with pleiotropic roles during embryonic development in vertebrates [4] and has long been proposed to play an important role during evolution [5,6]. RA levels are tightly controlled in the developing embryo, mainly by the expression of specific synthetizing (aldh1a) and degrading (cyp26) enzymes.…”

Section: Introductionmentioning

confidence: 99%

Altered retinoic acid signalling underpins dentition evolution

et al. 2015

View full text Add to dashboard Cite

Small variations in signalling pathways have been linked to phenotypic diversity and speciation. In vertebrates, teeth represent a reservoir of adaptive morphological structures that are prone to evolutionary change. Cyprinid fish display an impressive diversity in tooth number, but the signals that generate such diversity are unknown. Here, we show that retinoic acid (RA) availability influences tooth number size in Cyprinids. Heterozygous adult zebrafish heterozygous for the cyp26b1 mutant that encodes an enzyme able to degrade RA possess an extra tooth in the ventral row. Expression analysis of pharyngeal mesenchyme markers such as dlx2a and lhx6 shows lateral, anterior and dorsal expansion of these markers in RA-treated embryos, whereas the expression of the dental epithelium markers dlx2b and dlx3b is unchanged. Our analysis suggests that changes in RA signalling play an important role in the diversification of teeth in Cyprinids. Our work illustrates that through subtle changes in the expression of rate-limiting enzymes, the RA pathway is an active player of tooth evolution in fish

show abstract

Acquisition of Retinoic Acid Signaling Pathway and Innovation of the Chordate Body Plan

Cited by 41 publications

References 122 publications

Identification of All-trans-Retinol:All-trans-13,14-dihydroretinol Saturase

Identification of All-trans-Retinol:All-trans-13,14-dihydroretinol Saturase

Structural shifts of aldehyde dehydrogenase enzymes were instrumental for the early evolution of retinoid-dependent axial patterning in metazoans

Altered retinoic acid signalling underpins dentition evolution

Contact Info

Product

Resources

About