Pineal transducers in the course of evolution: Molecular organization, rhythmic metabolic activity and role.

Collin, Jean‐Pierre; Voisin, Pierre; Falcón, Jacky; Faure, Jean‐Pierre; Brisson, Paul; Defaye, Jean-René

doi:10.1679/aohc.52.suppl_441

Cited by 75 publications

(49 citation statements)

References 16 publications

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“…It converts the 24-h rhythm in environmental lighting into a 24-h rhythm in circulating melatonin, thereby providing a unique and valuable signal of the photic environment. The details of pineal evolution are not clear (4,5). However, it has been posited that an essential element was arylalkylamine N-acetyltransferase (AANAT; E.C.…”

mentioning

confidence: 99%

Drastic neofunctionalization associated with evolution of the timezyme AANAT 500 Mya

Falcón

Coon

Besseau

et al. 2013

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

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Melatonin (N-acetyl-5-methoxytrypamine) is the vertebrate hormone of the night: circulating levels at night are markedly higher than day levels. This increase is driven by precisely regulated increases in acetylation of serotonin in the pineal gland by arylalkylamine N-acetyltransferase (AANAT), the penultimate enzyme in the synthesis of melatonin. This unique essential role of AANAT in vertebrate timekeeping is recognized by the moniker the timezyme. AANAT is also found in the retina, where melatonin is thought to play a paracrine role. Here, we focused on the evolution of AANAT in early vertebrates. AANATs from Agnathans (lamprey) and Chondrichthyes (catshark and elephant shark) were cloned, and it was found that pineal glands and retinas from these groups express a form of AANAT that is compositionally, biochemically, and kinetically similar to AANATs found in bony vertebrates (VT-AANAT). Examination of the available genomes indicates that VT-AANAT is absent from other forms of life, including the Cephalochordate amphioxus. Phylogenetic analysis and evolutionary rate estimation indicate that VT-AANAT evolved from the nonvertebrate form of AANAT after the Cephalochordate-Vertebrate split over one-half billion years ago. The emergence of VT-AANAT apparently involved a dramatic acceleration of evolution that accompanied neofunctionalization after a duplication of the nonvertebrate AANAT gene. This scenario is consistent with the hypotheses that the advent of VT-AANAT contributed to the evolution of the pineal gland and lateral eyes from a common ancestral photodetector and that it was not a posthoc recruitment.E yes have evolved in all animals to facilitate interactions with the photic environment (1, 2). However, among animals, vertebrates are unique in that they also possess a photoneuroendocrine structure, the pineal gland (3). It converts the 24-h rhythm in environmental lighting into a 24-h rhythm in circulating melatonin, thereby providing a unique and valuable signal of the photic environment. The details of pineal evolution are not clear (4, 5). However, it has been posited that an essential element was arylalkylamine N-acetyltransferase (AANAT; E.C. 2.3.1.87), the penultimate enzyme in the melatonin biosynthesis pathway (6-8); this scenario is referred to as the AANAT hypothesis of pineal evolution (7,8).AANAT catalyzes the N-acetylation of arylalkylamines using acetyl CoA (AcCoA) as the acetyl group donor. The AANAT family, which belongs to the GCN5 superfamily (9, 10), is composed of two subfamilies termed vertebrate (VT) AANAT and nonvertebrate (NV) AANAT. † This nomenclature reflects the phylogenetic distribution of the family members (13-17). The most striking differences between VT-and NV-AANAT are found in regulatory and catalytic regions of the encoded proteins (Fig. 1), consistent with different metabolic roles (7,8).The NV-AANAT is thought to perform a detoxification function through acetylation of a broad range of endogenous and exogenous arylalkylamines and polyamines (13-16). It has been fo...

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mentioning

confidence: 99%

Drastic neofunctionalization associated with evolution of the timezyme AANAT 500 Mya

Falcón

Coon

Besseau

et al. 2013

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

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“…The retina and pineal gland probably arose via divergence from a common ancestral photoreceptive organ, and consistently, the pineal gland acts as a photosensory organ in the lowest vertebrate (1)(2)(3). In the course of vertebrate evolution, the physiological role of the pineal gland has been changed from a photosensory organ to a photoendocrinal organ in the lower vertebrates and eventually to a neuroendocrinal organ in mammals (4,5). Generally, the retina receives visual images and transmits them to the brain, whereas the primary role of the pineal gland is the rhythmic production of circulating melatonin, which regulates numerous physiological activities (6).…”

mentioning

confidence: 99%

Pineal expression-promoting element (PIPE), a cis- acting element, directs pineal-specific gene expression in zebrafish

Asaoka

Mano

Kojima

et al. 2002

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

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The pineal gland, sharing morphological and biochemical similarities with the retina, plays a unique and central role in the photoneuroendocrine system. The unique development of the pineal gland is directed by a specific combination of the expressed genes, but little is known about the regulatory mechanism underlying the pineal-specific gene expression. We isolated a 1.1-kbp fragment upstream of the zebrafish exo-rhodopsin (exorh) gene, which is expressed specifically in the pineal gland. Transgenic analysis using an enhanced green fluorescent protein reporter gene demonstrated that the proximal 147-bp region of the exorh promoter is sufficient to direct pineal-specific expression. This region contains three copies of a putative cone rod homeobox (Crx)͞Otx-binding site, which is known to be required for expression of both retina-and pineal-specific genes. Deletion and mutational analyses of the exorh promoter revealed that a previously uncharacterized sequence TGACCCCAATCT termed pineal expression-promoting element (PIPE) is required for pineal-specific promoter activity in addition to the Crx͞Otx-binding sites. By using the zebrafish rhodopsin (rh) promoter that drives retina-specific expression, we created a reporter construct having ectopic PIPE in the rh promoter at a position equivalent to that in the exorh promoter by introducing five nucleotide changes. Such a slight modification in the rh promoter induced ectopic enhanced green fluorescent protein expression in the pineal gland without affecting its retinal expression. These results identify PIPE as a critical cis-element contributing to the pineal-specific gene expression, in combination with the Crx͞Otx-binding site(s).

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“…The neuroendocrine terminals mentioned are formed by axons of the parapinealocytes bearing well developed outer segments. Therefore, the appearance of the pineal endocrine structures is not necessarily connected to the reduction of outer segments as seen in reptiles, birds or mammals (VOLLRATH, 1981, VIGH andVIGH-TEICHMANN, 1988;COLLIN et al, 1989). In our opinion, neurohormonal terminals of pineal organs represent an alternative efferentation besides a synaptic one, both being developed to a variable extent in the animals studied.…”

Section: Discussionmentioning

confidence: 68%

Two Components of the Pineal Organ in the Mink(Mustela vison): Their Structural Similarity to Submammalian Pineal Complexes and Calcification.

Vígh

Vigh-Teichmann

1992

Archives of Histology and Cytology

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Pineal transducers in the course of evolution: Molecular organization, rhythmic metabolic activity and role.

Cited by 75 publications

References 16 publications

Drastic neofunctionalization associated with evolution of the timezyme AANAT 500 Mya

Drastic neofunctionalization associated with evolution of the timezyme AANAT 500 Mya

Pineal expression-promoting element (PIPE), a cis- acting element, directs pineal-specific gene expression in zebrafish

Two Components of the Pineal Organ in the Mink(Mustela vison): Their Structural Similarity to Submammalian Pineal Complexes and Calcification.

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