Evolutionary aspects and enzymology of metazoan carotenoid cleavage oxygenases

Poliakov, Eugenia; Uppal, Sheetal; Rogozin, Igor B.; Gentleman, Susan; Redmond, T. Michael

doi:10.1016/j.bbalip.2020.158665

Cited by 21 publications

(17 citation statements)

References 97 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Because of the conserved nature of the PDPCK motif in the animal BCO/RPE65 clades of the carotenoid oxygenase superfamily, we postulated that the presence of this motif in any protein belonging to the family would predict palmitoylation of the protein. Recently, we confirmed our hypothesis by demonstrating that mouse BCO2 is also a palmitoylated protein [19]. In this paper, we demonstrate that PDPCK is a palmitoylation motif of BCO2 and that, similar to RPE65, BCO2 palmitoylation depends on the presence of substrate.…”

Section: Introductionsupporting

confidence: 80%

“…Carotenoid oxygenases act on hydrophobic substrates and their interaction with membrane and availability of substrate from membrane or lipid droplets is not completely known. Most metazoan carotenoid oxygenases contain the conserved PDPCK motif [12,19]. RPE65 retinoid isomerase is an enzyme which plays a crucial role in the regeneration of 11-cis-retinal (visual chromophore of rhodopsin) in the visual cycle of the retina [18,20,21].…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Palmitoylation of Metazoan Carotenoid Oxygenases

et al. 2020

Self Cite

View full text Add to dashboard Cite

Abundant in nature, carotenoids are a class of fat-soluble pigments with a polyene tetraterpenoid structure. They possess antioxidant properties and their consumption leads to certain health benefits in humans. Carotenoid cleavage oxygenases (CCOs) are a superfamily of enzymes which oxidatively cleave carotenoids and they are present in all kingdoms of life. Complexity of CCO evolution is high. For example, in this study we serendipitously found a new family of eukaryotic CCOs, the apocarotenoid oxygenase-like (ACOL) family. This family has several members in animal genomes and lacks the animal-specific amino acid motif PDPCK. This motif is likely to be associated with palmitoylation of some animal CCOs. We recently demonstrated that two mammalian members of the carotenoid oxygenase family retinal pigment epithelial-specific 65 kDa protein (RPE65) and beta-carotene oxygenase 2 (BCO2) are palmitoylated proteins. Here we used the acyl-resin-assisted capture (acyl-RAC) method to demonstrate protein palmitoylation and immunochemistry to localize mouse BCO2 (mBCO2) in COS7 cell line in the absence and presence of its substrate β-carotene. We demonstrate that mBCO2 palmitoylation depends on the evolutionarily conserved motif PDPCK and that metazoan family members lacking the motif (Lancelet beta-carotene oxygenase-like protein (BCOL) and Acropora ACOL) are not palmitoylated. Additionally, we observed that the palmitoylation status of mBCO2 and its membrane association depend on the presence of its substrate β-carotene. Based on our results we conclude that most metazoan carotenoid oxygenases retain the evolutionarily conserved palmitoylation PDPCK motif to target proteins to internal membranes depending on substrate status. Exceptions are in the secreted BCOL subfamily and the strictly cytosolic ancient ACOL subfamily of carotenoid oxygenases.

show abstract

Section: Introductionsupporting

confidence: 80%

Section: Introductionmentioning

confidence: 99%

Palmitoylation of Metazoan Carotenoid Oxygenases

et al. 2020

Self Cite

View full text Add to dashboard Cite

show abstract

“…β-carotene oxygenase 1 (Bco1) symmetrically cleaves β-carotene to produce vitamin A, a precursor of retinoic acid; whereas β-carotene oxygenase 2 (Bco2) cleaves a variety of carotenoids in an asymmetric fashion, often leading to their degradation ( Widjaja-Adhi et al, 2015 ; Li et al, 2017 ; Harrison and Kopec, 2020 ; Poliakov et al, 2020 ). bco1 and bco2b were more abundant in tissue containing xanthophores than erythrophores (log 2 FC = 4.9, 2.1; q = 9.6E-23, 8.9E-8); a third locus, bco2l was similarly abundant at both sites ( Supplementary file 1 — Table 1 ).…”

Section: Resultsmentioning

confidence: 99%

Development and genetics of red coloration in the zebrafish relative Danio albolineatus

Huang

Lewis

Foster

et al. 2021

eLife

View full text Add to dashboard Cite

Animal pigment patterns play important roles in behavior and, in many species, red coloration serves as an honest signal of individual quality in mate choice. Among Danio fishes, some species develop erythrophores, pigment cells that contain red ketocarotenoids, whereas other species, like zebrafish (D. rerio) only have yellow xanthophores. Here, we use pearl danio (D. albolineatus) to assess the developmental origin of erythrophores and their mechanisms of differentiation. We show that erythrophores in the fin of D. albolineatus share a common progenitor with xanthophores and maintain plasticity in cell fate even after differentiation. We further identify the predominant ketocarotenoids that confer red coloration to erythrophores and use reverse genetics to pinpoint genes required for the differentiation and maintenance of these cells. Our analyses are a first step toward defining the mechanisms underlying the development of erythrophore-mediated red coloration in Danio and reveal striking parallels with the mechanism of red coloration in birds.

show abstract

“…In high-salinity waters, transcripts related to retinal metabolic processes were signi cantly up-regulated; A. salina signi cantly up-regulated ninaB homologous genes in high-salinity media. Many diverse metazoan species contain ninaB homolog genes ( Figure S3 in Additional File 3), which are associated with the synthesis of visual pigment and oxidative stress [74][75][76]. Moreover, the upregulation of genes related to oxidative stress suggests that A. salina can adapt to waters simultaneously high in salinity and low in oxygen.…”

Section: Discussionmentioning

confidence: 99%

Tolerance at the genetic level of the brine shrimp Artemia salina to a wide range of salinity

Lee¹,

Park²

2020

Preprint

View full text Add to dashboard Cite

Background: The brine shrimp Artemia salina can thrive in a variety of salinities and is commonly distributed in natural hypersaline lakes and solar salterns. The zooplankter A. salina proves to be a filter feeder, consuming the alga Dunaliella and prokaryotes and plays a critical role in the hypersaline food web. However, the high salinity adaptation mechanisms of A. salina remain poorly understood through transcriptome analysis. Here, we examined the gene expression patterns of A. salina adults that were salt-adapted for 2–4 weeks at five salinities (35, 50, 100, 150, and 230 psu), and generated long-read isoform sequencing (IsoSeq) data to construct a high-quality transcriptome assembly of A. salina. The patterns of A. salina along the salinity gradient provide evidence for halotolerant and euryhaline adaptations at the genetic level. Results: We confirmed that the activity of sodium/potassium ATPase was up-regulated at the genetic level in high salinity waters. Interestingly, genes related to beta-mannosidase and mannose activities were also up-regulated, suggesting that mannose and mannose derivatives may be accumulated as organic osmolytes. Alternatively, considering that glucose and galactose-related activities were suppressed at high salinities, mannose may be the primary sugar involved in the glycolytic pathway under such conditions. This result further supports the theory that mannose is the main energy source used by A. salina in highly saline environments. The gene expression patterns of A. salina may also be affected by increased thickness of the cuticle, increased numbers of mitochondria, and low dissolved oxygen in high salinity waters. Furthermore, the cellular response of A. salina to acclimation to intermediate salinities depends on the number and type of genes expressed; differential expression patterns are likely to fluctuate at the population level. Conclusions: Our results provide a high-quality transcriptome assembly of the cosmopolitan brine shrimp Artemia salina at five different salinities (35, 50, 100, 150, and 230 psu) for the first time. The gene expression patterns of salt-adapted A. salina display greater osmoregulation process complexity than we thought. Furthermore, A. salina represents a potential model organism to study locally adapted populations at various salinities.

show abstract

Evolutionary aspects and enzymology of metazoan carotenoid cleavage oxygenases

Cited by 21 publications

References 97 publications

Palmitoylation of Metazoan Carotenoid Oxygenases

Palmitoylation of Metazoan Carotenoid Oxygenases

Development and genetics of red coloration in the zebrafish relative Danio albolineatus

Tolerance at the genetic level of the brine shrimp Artemia salina to a wide range of salinity

Contact Info

Product

Resources

About