Photoreceptor-specific efficiencies of ?-carotene, zeaxanthin and lutein for photopigment formation deduced from receptor mutant Drosophila melanogaster

Stark, William S.; Schilly, D.; Christianson, J. Scott; Bone, Richard A.; Landrum, John T.

doi:10.1007/bf00192014

Cited by 14 publications

(17 citation statements)

References 34 publications

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“…In Drosophila, vitamin A is only needed for vision, as animals grown on medium lacking vitamin A show only nonlethal visual deficits (16). Thus, the Drosophila experimental system is easily amenable to the genetic and molecular analysis of the components and cellular sites responsible for vitamin A metabolism.…”

mentioning

confidence: 99%

Drosophila NinaB and NinaD Act Outside of Retina to Produce Rhodopsin Chromophore

Gu¹,

Yang²,

Mitchell

et al. 2004

Journal of Biological Chemistry

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The Drosophila ninaB gene encodes a ␤,␤-carotene-15,15 -oxygenase responsible for the centric cleavage of ␤-carotene that produces the retinal chromophore of rhodopsin. The ninaD gene encodes a membrane receptor required for efficient use of ␤-carotene. Despite their importance to the synthesis of visual pigment, we show that these genes are not active in the retina. Mosaic analysis shows that ninaB and ninaD are not required in the retina, and exclusive retinal expression of either gene, or both genes simultaneously, does not support rhodopsin biogenesis. In contrast, neuron-specific expression of ninaB and ninaD allows for rhodopsin biogenesis. Additional directed expression studies failed to identify other tissues supporting ninaB activity in rhodopsin biogenesis. These results show that nonretinal sites of NinaB ␤,␤-carotene-15,15 -oxygenase activity, likely neurons of the central nervous system, are essential for production of the visual chromophore. Retinal or another C 20 retinoid, not members of the ␤-carotene family of C 40 carotenoids, are supplied to photoreceptors for rhodopsin biogenesis.Mutants in eight Drosophila genes, designated ninaA through ninaH, are characterized by reduced rhodopsin levels in photoreceptors and altered electroretinograms (1). The opsin protein component of rhodopsin is coded by the ninaE gene (2, 3). The low rhodopsin phenotypes observed in other nina mutants are caused by deficits in the post-translational rhodopsin maturation process. For example, ninaA encodes a molecular chaperone required for movement of newly synthesized rhodopsin from the endoplasmic reticulum to the photosensitive rhabdomeric membranes (4, 5). In the case of ninaB and ninaD, defective rhodopsin production is the result of a failure to generate the chromophore of rhodopsin, 3-OH retinal (6).Animal species usually obtain retinals in their food. Plants and microorganisms produce C 40 carotenoids such as ␤-carotene and zeaxanthin, which animals metabolize to C 20 retinoids. In Drosophila, the ninaD gene encodes a membrane "scavenger" receptor proposed to mediate the cellular uptake of carotenoids (7). The ninaB gene encodes a ␤,␤-carotene-15,15Ј-oxygenase (BCO) 1 responsible for the centric cleavage of ␤-carotene to form retinal (8). This enzyme was originally named as a ␤-carotene dioxygenase. It has now been renamed BCO (9) in light of recent data showing related enzymes act as monooxygenases (10).In vertebrates, vitamin A is essential for development and differentiation processes as well as its role in vision. The availability of vitamin A for metabolic processes is governed by multiple factors, including dietary absorption, transport, metabolism, and storage (11). A human BCO is expressed in the retinal pigment epithelium and also in the kidney, intestine, liver, brain, stomach, and testis (12, 13), suggesting that the processing of dietary carotenoids occurs in a variety of vertebrate tissues. Additional studies show that centric cleavage of ␤-carotene plays a major role in the processing of carote...

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confidence: 99%

Drosophila NinaB and NinaD Act Outside of Retina to Produce Rhodopsin Chromophore

Gu¹,

Yang²,

Mitchell

et al. 2004

Journal of Biological Chemistry

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“…5 to account for the current information regarding (3S)-3-hydroxyretinal biosynthesis in Drosophila. Xanthophylls, such as lutein and zeaxanthin that are hydroxylated at the C-3 position of the retinoid ring and ␤-carotene, are the major dietary source of chromophore precursors (11,16). All naturally occurring xanthophylls are in the 3R,3ЈR configuration thereby ruling out the possibility of obtaining retinoid species in 3S configuration by direct cleavage of such xanthophylls by an oxygenase.…”

Section: Discussionmentioning

confidence: 99%

The Role of Drosophila ninaG Oxidoreductase in Visual Pigment Chromophore Biogenesis

Ahmad

Joyce

Boggess

et al. 2006

Journal of Biological Chemistry

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We previously reported (Sarfare, S., Ahmad, S. T., Joyce, M. V., Boggess, B., and O'Tousa, J. E. (2005) J. Biol. Chem. 280, 11895-11901) that the Drosophila ninaG gene encodes an oxidoreductase involved in the biosynthesis of the (3S)-3-hydroxyretinal serving as chromophore for Rh1 rhodopsin and that ninaG mutant flies expressing Rh4 as the major opsin accumulate large amounts of a different retinoid. Here, we show that this unknown retinoid is 11-cis-3-hydroxyretinol. Reversed phase high performance liquid chromatography coupled with a photodiode array UV-visible absorbance detector and mass spectrometer revealed a major product eluting at a retention time, t r , of 3.5 min with a max of ϳ324 nm and with a base peak in the mass spectrum at m/z 285. These observations are identical with those of the 3-hydroxyretinol standard. The base peak in the electrospray ionization mass spectrum arises from the loss of a water molecule from the protonated molecule at m/z 303 because of fragmentation in the ion source. These results suggest that 11-cis-3-hydroxyretinol is an intermediate required for chromophore biogenesis in Drosophila. We further show that ninaG mutants fed on retinal as the sole source of vitamin A are able to synthesize 3-hydroxyretinoids. Thus, the NinaG oxidoreductase is not responsible for the initial hydroxylation of the retinal ring but rather acts in a subsequent step in chromophore production. These data are used to review chromophore biosynthesis and propose that NinaG acts in the conversion of (3R)-3-hydroxyretinol to the 3S enantiomer.Photoisomerization of a retinoid chromophore covalently linked to the apoprotein opsin underlies the light-sensing ability of rhodopsins. Animals lack the ability to synthesize retinoids de novo and, therefore, derive retinoids from carotenoids present in the diet. In insects, three kinds of vitamin A derivatives, retinal, (3R)-3-hydroxyretinal, and (3S)-3-hydroxyretinal, function as chromophores (1). The Dipteran suborder Cyclorrapha that includes Drosophila is the only suborder described so far that utilizes (3S)-3-hydroxyretinal as the Rh1 rhodopsin chromophore (2). The use of (3S)-3-hydroxyretinal occurs in visual pigments exhibiting both UV and visible light sensitivity. This led to the suggestion that UV light sensitivity is because of the unique ability of (3S)-3-hydroxyretinal to accept energy transferred from a UV-sensitizing pigment (1).The Drosophila ninaG mutant is characterized by an abnormal electroretinogram response lacking the prolonged depolarization afterpotential. The lack of prolonged depolarization afterpotential, a characteristic of a group of "nina" 2 genes, is a manifestation of low levels of the major opsin, Rh1, expressed in the R1-6 photoreceptor cells (3). Low Rh1 rhodopsin in ninaG mutants is not due to defects in Rh1 opsin transcription, but rather, the ability to synthesize the Rh1 chromophore is defective. However, the ninaG defect does not affect the expression of minor opsins Rh4 and Rh6 (4). Rh4 and Rh6 are expressed in the R7 a...

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“…Probably the lutein and zeaxanthin contained in yellow cornmeal serve as adequate sources of carotenoids ; however, to be certain of sufficient vitamin A, we supplemented our fly food with β-carotene at 0n125 mg ml −" . This is the lowest dose found to maximize visual sensitivity and visual pigment (Stark and Johnson, 1980 ;Stark et al, 1990) for flies reared from egg to adult on an otherwise retinoid-deficient medium. Retinoid deprivation was achieved by rearing flies from egg to adult on Sang's medium without any retinoids (Stark, 1977).…”

Section: Animals and Retinoid Manipulationsmentioning

confidence: 99%

“…We maintained flies on our standard medium, adequate for full levels of visual pigment (Stark and Johnson, 1980 ;Stark et al, 1990) and visual function (Stark, Ivanyshyn and Greenberg, 1977 ;Stark et al, 1990). Probably the lutein and zeaxanthin contained in yellow cornmeal serve as adequate sources of carotenoids ; however, to be certain of sufficient vitamin A, we supplemented our fly food with β-carotene at 0n125 mg ml −" .…”

Section: Animals and Retinoid Manipulationsmentioning

confidence: 99%

Control ofDrosophilaRetinoid and Fatty Acid Binding Glycoprotein Expression by Retinoids and Retinoic Acid: Northern, Western and Immunocytochemical Analyses

Shim

Picking

Kutty

et al. 1997

Experimental Eye Research

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Photoreceptor-specific efficiencies of ?-carotene, zeaxanthin and lutein for photopigment formation deduced from receptor mutant Drosophila melanogaster

Cited by 14 publications

References 34 publications

Drosophila NinaB and NinaD Act Outside of Retina to Produce Rhodopsin Chromophore

Drosophila NinaB and NinaD Act Outside of Retina to Produce Rhodopsin Chromophore

The Role of Drosophila ninaG Oxidoreductase in Visual Pigment Chromophore Biogenesis

Control ofDrosophilaRetinoid and Fatty Acid Binding Glycoprotein Expression by Retinoids and Retinoic Acid: Northern, Western and Immunocytochemical Analyses

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