Unique arylalkylamine <i>N</i>-acetyltransferase-2 polymorphism in Salmonids and profound variations in thermal stability and catalytic efficiency conferred by two residues

Cazaméa-Catalan, Damien; Magnanou, Elodie; Helland, Ronny; Bœuf, Gilles; Falcón, Jack; Jørgensen, Even H.

doi:10.1242/jeb.080960

Cited by 17 publications

(14 citation statements)

References 52 publications

(61 reference statements)

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“…Aanat enzymes of vertebrates usually display a significantly higher catalytic efficiency for indolethylamines versus phenylethylamines . We bring here evidence that Aanat1 enzymes acetylated both indolethylamines and phenylethylamines in accordance with our previous findings in other species .…”

Section: Discussionsupporting

confidence: 90%

“…S2). These valine and isoleucine are involved in thermal stability and catalytic efficiency of teleost Aanat2 . In a thorough analysis of the available teleost's Aanat sequences, we found that these residues are highly conserved among teleost Aanat2 and, when not present, replaced by a valine while the corresponding lysine and methionine found in Aanat1a and Aanat1b are specific of this family and of Sarcopterygii Aanats.…”

Section: Resultsmentioning

confidence: 81%

“…Aanat1 and Aanat2 display different kinetics and mechanisms of regulation . Pineal Aanat2 has high affinity for indolethylamines, exhibits a species‐specific temperature dependency and always follows a nocturnal activity pattern . In contrast, retinal Aanat1 has affinity for both indoleamines and phenylethylamines, and a similar response to temperature in all the species investigated so far.…”

Section: Introductionmentioning

confidence: 97%

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Subfunctionalization of arylalkylamine N‐acetyltransferases in the sea bass Dicentrarchus labrax: two‐ones for one two

Paulin

Cazaméa-Catalan

Zilberman-Peled

et al. 2015

Journal of Pineal Research

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Melatonin is an important component of the vertebrates circadian system, synthetized from serotonin by the successive action of the arylalkylamine N-acetyltransferase (Aanat: serotonin→N-acetylserotonin) and acetylserotonin-O-methyltransferase (Asmt: N-acetylserotonin→melatonin). Aanat is responsible for the daily rhythm in melatonin production. Teleost fish are unique because they express two Aanat genes, aanat1 and aanat2, mainly expressed in the retina and pineal gland, respectively. In silico analysis indicated that the teleost-specific whole-genome duplication generated Aanat1 duplicates (aanat1a and aanat1b); some fish express both of them, while others express either one of the isoforms. Here, we bring the first information on the structure, function, and distribution of Aanat1a and Aanat1b in a teleost, the sea bass Dicentrarchus labrax. Aanat1a and Aanat1b displayed a wide and distinct distribution in the nervous system and peripheral tissues, while Aanat2 appeared as a pineal enzyme. Co-expression of Aanats with asmt was found in the pineal gland and the three retinal nuclear layers. Enzyme kinetics indicated subtle differences in the affinity and catalytic efficiency of Aanat1a and Aanat1b for indolethylamines and phenylethylamines, respectively. Our data are consistent with the idea that Aanat2 is a pineal enzyme involved in melatonin production, while Aanat1 enzymes have a broader range of functions including melatonin synthesis in the retina, and catabolism of serotonin and dopamine in the retina and other tissues. The data are discussed in light of the recently uncovered roles of N-acetylserotonin and N-acetyldopamine as antioxidants, neuroprotectants, and modulators of cell proliferation and enzyme activities.

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Section: Discussionsupporting

confidence: 90%

Section: Resultsmentioning

confidence: 81%

Section: Introductionmentioning

confidence: 97%

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Subfunctionalization of arylalkylamine N‐acetyltransferases in the sea bass Dicentrarchus labrax: two‐ones for one two

Paulin

Cazaméa-Catalan

Zilberman-Peled

et al. 2015

Journal of Pineal Research

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“…The encoded proteins (206 and 207 aa) exhibited the two defining features of the GCN5 N-acetyltransferase superfamily, motifs A and B (SI Appendix, Fig. S1) (9,(22)(23)(24)(25)(26)(27)(28)(29). In addition, the sequences exhibited defining characteristics of the VT-AANATs of bony vertebrates, including motifs C and D, PKA sites nested in 14-3-3 binding domains, a Cys-ProLeu peptide sequence in a floppy loop within the binding region, and closely positioned histidine residues in the active site.…”

Section: Resultsmentioning

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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“…(iii) In cultured pineal organs, both cAMP production and AANAT activity display the same pattern in response to temperature; this is a species-dependent process (5). It is also a cellular-mediated process because the response of AANAT activity to temperature variation differs if measured on the native (ie, in situ) or recombinant enzymes (24,25). (iv) In mammals, temperature sensing is mediated by members of the Transient Receptor Potential (TRP) channels family (TRPA1, TRPV1-4 and TRPM8), which are permeable to Ca 2ϩ (26,27), and activate at different ranges of temperature (28).…”

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confidence: 99%

In the Heat of the Night: Thermo-TRPV Channels in the Salmonid Pineal Photoreceptors and Modulation of Melatonin Secretion

et al. 2015

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Photoperiod plays an essential role in the synchronization of metabolism, physiology, and behavior to the cyclic variations of the environment. In vertebrates, information is relayed by the pineal cells and translated into the nocturnal production of melatonin. The duration of this signal corresponds to the duration of the night. In fish, the pinealocytes are true photoreceptors in which the amplitude of the nocturnal surge is modulated by temperature in a species-dependent manner. Thus, the daily and annual variations in the amplitude and duration of the nocturnal melatonin signal provide information on daily and calendar time. Both light and temperature act on the activity of the penultimate enzyme in the melatonin biosynthesis pathway, the arylalkylamine N-acetyltransferase (serotonin → N-acetylserotonin). Although the mechanisms of the light/dark regulation of melatonin secretion are quite well understood, those of temperature remain unelucidated. More generally, the mechanisms of thermoreception are unknown in ectotherms. Here we provide the first evidence that two thermotransient receptor potential (TRP) channels, TRPV1 and TRPV4, are expressed in the pineal photoreceptor cells of a teleost fish, in which they modulate melatonin secretion in vitro. The effects are temperature dependent, at least for TRPV1. Our data support the idea that the pineal of fish is involved in thermoregulation and that the pineal photoreceptors are also thermoreceptors. In other nervous and nonnervous tissues, TRPV1 and TRPV4 display a ubiquitous but quantitatively variable distribution. These results are a fundamental step in the elucidation of the mechanisms of temperature transduction in fish.

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Unique arylalkylamine N-acetyltransferase-2 polymorphism in Salmonids and profound variations in thermal stability and catalytic efficiency conferred by two residues

Cited by 17 publications

References 52 publications

Subfunctionalization of arylalkylamine N‐acetyltransferases in the sea bass Dicentrarchus labrax: two‐ones for one two

Subfunctionalization of arylalkylamine N‐acetyltransferases in the sea bass Dicentrarchus labrax: two‐ones for one two

Drastic neofunctionalization associated with evolution of the timezyme AANAT 500 Mya

In the Heat of the Night: Thermo-TRPV Channels in the Salmonid Pineal Photoreceptors and Modulation of Melatonin Secretion

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