{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,7]],"date-time":"2025-12-07T23:56:08Z","timestamp":1765151768465,"version":"3.41.2"},"reference-count":51,"publisher":"The Company of Biologists","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:title>Summary<\/jats:title>\n               <jats:p>Melatonin contributes to synchronizing major biological and behavioral functions to the cyclic changes in the environment. The arylalkylamine N-acetyltransferase (AANAT) is responsible for a daily rhythm in melatonin secretion. Teleost possess two enzyme forms, AANAT1 and AANAT2, preferentially expressed in the retina and pineal organ, respectively. The concomitant action of light and temperature shapes the daily and seasonal changes in melatonin secretion: the former controls duration while the latter modulates amplitude. Investigating the respective roles of light and temperature is particularly relevant in the context of a global warming likely to affect the way fish decode and anticipate seasonal changes with dramatic consequences on their physiology and behavior. Here we investigated the impact of temperature on pineal melatonin secretion of a migratory species, the Arctic charr (Salvelinus alpinus), the northernmost living and cold adapted salmonid. We show that temperature impacts directly melatonin production in cultured pineal organs. We also show that one organ expresses two AANAT2 transcripts displaying high similarity between them and with trout Oncorhynchus mykiss AANAT2, differing by only two amino acid sites. We compared the kinetics and 3D models of these enzymes as well as of a chimeric construct, particularly with regard to their response to temperature. Our study brings interesting and totally new information on the evolutionary diversity of AANAT enzymes in Teleost and on the role played by specific residues in the catalytic properties of the enzymes.<\/jats:p>","DOI":"10.1242\/jeb.080960","type":"journal-article","created":{"date-parts":[[2013,2,8]],"date-time":"2013-02-08T07:12:22Z","timestamp":1360307542000},"source":"Crossref","is-referenced-by-count":15,"title":["Unique arylalkylamine <i>N<\/i>-acetyltransferase-2 polymorphism in Salmonids and profound variations in thermal stability and catalytic efficiency conferred by two residues"],"prefix":"10.1242","author":[{"given":"Damien","family":"Cazam\u00e9a-Catalan","sequence":"first","affiliation":[{"name":"Universit\u00e9 Pierre et Marie Curie-Paris;"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elodie","family":"Magnanou","sequence":"additional","affiliation":[{"name":"CNRS, Biologie Int\u00e9grative des Organismes Marins;"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ronny","family":"Helland","sequence":"additional","affiliation":[{"name":"University of Troms\u00f8;"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Laurence","family":"Besseau","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Pierre et Marie Curie-Paris;"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gilles","family":"Boeuf","sequence":"additional","affiliation":[{"name":"Mus\u00e9um National d'Histoire Naturelle"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jack","family":"Falc\u00f3n","sequence":"additional","affiliation":[{"name":"CNRS, Biologie Int\u00e9grative des Organismes Marins;"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Even H.","family":"J\u00f8rgensen","sequence":"additional","affiliation":[{"name":"University of Troms\u00f8;"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","published-online":{"date-parts":[[2013,1,1]]},"reference":[{"key":"2021042507020244300_R1","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.mce.2006.03.021","article-title":"Mechanism of pineal-specific gene expression: the role of E-box and photoreceptor conserved elements","volume":"252","author":"Appelbaum","year":"2006","journal-title":"Mol. Cell. Endocrinol."},{"key":"2021042507020244300_R2","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1093\/bioinformatics\/bti770","article-title":"The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling","volume":"22","author":"Arnold","year":"2006","journal-title":"Bioinformatics"},{"key":"2021042507020244300_R3","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1097\/00001756-200002070-00006","article-title":"Melatonin synthesis: arylalkylamine N-acetyltransferases in trout retina and pineal organ are different","volume":"11","author":"Benyassi","year":"2000","journal-title":"Neuroreport"},{"key":"2021042507020244300_R4","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.ygcen.2010.07.003","article-title":"Environmental endocrinology of salmon smoltification","volume":"170","author":"Bj\u00f6rnsson","year":"2011","journal-title":"Gen. Comp. Endocrinol."},{"key":"2021042507020244300_R5","doi-asserted-by":"crossref","first-page":"5027","DOI":"10.1111\/j.1365-294X.2012.05725.x","article-title":"Functional diversity of teleost arylalkylamine N-acetyltransferase-2: is the timezyme evolution driven by habitat temperature?","volume":"21","author":"Cazam\u00e9a-Catalan","year":"2012","journal-title":"Mol. Ecol."},{"key":"2021042507020244300_R6","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.mce.2006.03.039","article-title":"Evolution of arylalkylamine N-acetyltransferase: emergence and divergence","volume":"252","author":"Coon","year":"2006","journal-title":"Mol. Cell. Endocrinol."},{"key":"2021042507020244300_R7","doi-asserted-by":"crossref","first-page":"9076","DOI":"10.1074\/jbc.274.13.9076","article-title":"Two arylalkylamine N-acetyltransferase genes mediate melatonin synthesis in fish","volume":"274","author":"Coon","year":"1999","journal-title":"J. Biol. Chem."},{"key":"2021042507020244300_R8","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1083\/jcb.200611141","article-title":"Error bars in experimental biology","volume":"177","author":"Cumming","year":"2007","journal-title":"J. Cell Biol."},{"key":"2021042507020244300_R9","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1023\/A:1007447417546","article-title":"Critical thermal minima and maxima of three freshwater game-fish species acclimated to constant temperatures","volume":"51","author":"Currie","year":"1998","journal-title":"Environ. Biol. Fishes"},{"key":"2021042507020244300_R10","doi-asserted-by":"crossref","first-page":"3045","DOI":"10.1074\/jbc.273.5.3045","article-title":"Kinetic analysis of the catalytic mechanism of serotonin N-acetyltransferase (EC 2.3.1.87)","volume":"273","author":"De Angelis","year":"1998","journal-title":"J. Biol. Chem."},{"key":"2021042507020244300_R11","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/S0301-0082(98)00078-1","article-title":"Cellular circadian clocks in the pineal","volume":"58","author":"Falc\u00f3n","year":"1999","journal-title":"Prog. Neurobiol."},{"key":"2021042507020244300_R12","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1159\/000124778","article-title":"Rhythmic melatonin biosynthesis in a photoreceptive pineal organ: a study in the pike","volume":"45","author":"Falc\u00f3n","year":"1987","journal-title":"Neuroendocrinology"},{"key":"2021042507020244300_R13","doi-asserted-by":"crossref","first-page":"1943","DOI":"10.1523\/JNEUROSCI.09-06-01943.1989","article-title":"Regulation of melatonin secretion in a photoreceptive pineal organ: an in vitro study in the pike","volume":"9","author":"Falc\u00f3n","year":"1989","journal-title":"J. Neurosci."},{"key":"2021042507020244300_R14","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1159\/000126792","article-title":"Rhythmic secretion of melatonin by the superfused pike pineal organ: thermo- and photoperiod interaction","volume":"60","author":"Falc\u00f3n","year":"1994","journal-title":"Neuroendocrinology"},{"key":"2021042507020244300_R15","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1007\/s004240050149","article-title":"Partial characterization of serotonin N-acetyltransferases from northern pike (Esox lucius, L.) pineal organ and retina: effects of temperature","volume":"432","author":"Falc\u00f3n","year":"1996","journal-title":"Pflugers Arch."},{"key":"2021042507020244300_R16","doi-asserted-by":"crossref","first-page":"1804","DOI":"10.1210\/endo.142.5.8129","article-title":"Regulation of arylalkylamine N-acetyltransferase-2 (AANAT2, EC 2.3.1.87) in the fish pineal organ: evidence for a role of proteasomal proteolysis","volume":"142","author":"Falc\u00f3n","year":"2001","journal-title":"Endocrinology"},{"key":"2021042507020244300_R17","first-page":"243","article-title":"Molecular and cellular regulation of pineal organ responses","volume-title":"Sensory Systems Neuroscience \u2013 Fish Physiology","author":"Falc\u00f3n","year":"2007"},{"key":"2021042507020244300_R18","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.ygcen.2009.04.026","article-title":"Current knowledge on the melatonin system in teleost fish","volume":"165","author":"Falc\u00f3n","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"2021042507020244300_R19","doi-asserted-by":"crossref","first-page":"11476","DOI":"10.1073\/pnas.95.19.11476","article-title":"Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes","volume":"95","author":"Fields","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042507020244300_R20","doi-asserted-by":"crossref","first-page":"8083","DOI":"10.1073\/pnas.141118798","article-title":"Role of a pineal cAMP-operated arylalkylamine N-acetyltransferase\/14-3-3-binding switch in melatonin synthesis","volume":"98","author":"Ganguly","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042507020244300_R21","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.1126\/science.279.5355.1358","article-title":"Melatonin production: proteasomal proteolysis in serotonin N-acetyltransferase regulation","volume":"279","author":"Gastel","year":"1998","journal-title":"Science"},{"key":"2021042507020244300_R22","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/0016-6480(88)90307-3","article-title":"Examination of in vitro melatonin secretion from superfused trout (Salmo gairdneri) pineal organs maintained under diel illumination or continuous darkness","volume":"71","author":"Gern","year":"1988","journal-title":"Gen. Comp. Endocrinol."},{"key":"2021042507020244300_R23","doi-asserted-by":"crossref","first-page":"4895","DOI":"10.1210\/endo.140.10.6975","article-title":"Zebrafish serotonin N-acetyltransferase-2: marker for development of pineal photoreceptors and circadian clock function","volume":"140","author":"Gothilf","year":"1999","journal-title":"Endocrinology"},{"key":"2021042507020244300_R24","doi-asserted-by":"crossref","first-page":"3320","DOI":"10.1093\/nar\/gkg556","article-title":"ESPript\/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins","volume":"31","author":"Gouet","year":"2003","journal-title":"Nucleic Acids Res."},{"key":"2021042507020244300_R25","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/S1097-2765(00)80171-9","article-title":"Melatonin biosynthesis: the structure of serotonin N-acetyltransferase at 2.5 \u00c5 resolution suggests a catalytic mechanism","volume":"3","author":"Hickman","year":"1999","journal-title":"Mol. Cell"},{"key":"2021042507020244300_R26","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/S0092-8674(00)80745-X","article-title":"The structural basis of ordered substrate binding by serotonin N-acetyltransferase: enzyme complex at 1.8 \u00c5 resolution with a bisubstrate analog","volume":"97","author":"Hickman","year":"1999","journal-title":"Cell"},{"key":"2021042507020244300_R27","doi-asserted-by":"crossref","first-page":"3207","DOI":"10.1021\/bi962664k","article-title":"Evolution of lactate dehydrogenase-A homologs of barracuda fishes (genus Sphyraena) from different thermal environments: differences in kinetic properties and thermal stability are due to amino acid substitutions outside the active site","volume":"36","author":"Holland","year":"1997","journal-title":"Biochemistry"},{"key":"2021042507020244300_R28","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.ygcen.2007.06.013","article-title":"Lack of circadian regulation of in vitro melatonin release from the pineal organ of salmonid teleosts","volume":"154","author":"Iigo","year":"2007","journal-title":"Gen. Comp. Endocrinol."},{"key":"2021042507020244300_R29","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1093\/molbev\/msh021","article-title":"Evolutionary convergence in adaptation of proteins to temperature: A4-lactate dehydrogenases of Pacific damselfishes (Chromis spp.)","volume":"21","author":"Johns","year":"2004","journal-title":"Mol. Biol. Evol."},{"key":"2021042507020244300_R30","doi-asserted-by":"crossref","first-page":"2577","DOI":"10.1002\/bip.360221211","article-title":"Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features","volume":"22","author":"Kabsch","year":"1983","journal-title":"Biopolymers"},{"key":"2021042507020244300_R31","first-page":"307","article-title":"The melatonin rhythm-generating enzyme: molecular regulation of serotonin N-acetyltransferase in the pineal gland","volume":"52","author":"Klein","year":"1997","journal-title":"Recent Prog. Horm. Res."},{"key":"2021042507020244300_R32","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1046\/j.1365-2826.2003.01000.x","article-title":"14-3-3 proteins in pineal photoneuroendocrine transduction: how many roles?","volume":"15","author":"Klein","year":"2003","journal-title":"J. Neuroendocrinol."},{"key":"2021042507020244300_R33","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1093\/bioinformatics\/btp187","article-title":"DnaSP v5: a software for comprehensive analysis of DNA polymorphism data","volume":"25","author":"Librado","year":"2009","journal-title":"Bioinformatics"},{"key":"2021042507020244300_R34","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.2108\/zsj.20.1011","article-title":"Variations in plasma melatonin levels of the rainbow trout (Oncorhynchus mykiss) under various light and temperature conditions","volume":"20","author":"Masuda","year":"2003","journal-title":"Zool. Sci."},{"key":"2021042507020244300_R35","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1007\/BF00191463","article-title":"Regulation of melatonin production by light, darkness, and temperature in the trout pineal","volume":"170","author":"Max","year":"1992","journal-title":"J. Comp. Physiol. A"},{"key":"2021042507020244300_R36","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1111\/j.1095-8649.2009.02500.x","article-title":"Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species","volume":"76","author":"Migaud","year":"2010","journal-title":"J. Fish Biol."},{"key":"2021042507020244300_R37","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1016\/j.jtherbio.2007.03.004","article-title":"Seasonal variation in the temperature preference of Arctic charr (Salvelinus alpinus)","volume":"32","author":"Mortensen","year":"2007","journal-title":"J. Therm. Biol."},{"key":"2021042507020244300_R38","first-page":"R743","article-title":"Summer osmoregulatory capacity of the world's northernmost living salmonid","volume":"272","author":"Nilssen","year":"1997","journal-title":"Am. J. Physiol."},{"key":"2021042507020244300_R39","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/S0092-8674(01)00316-6","article-title":"Crystal structure of the 14-3-3zeta:serotonin N-acetyltransferase complex: a role for scaffolding in enzyme regulation","volume":"105","author":"Obsil","year":"2001","journal-title":"Cell"},{"key":"2021042507020244300_R40","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1111\/j.1095-8649.2009.02484.x","article-title":"Temperature and salmonid reproduction: implications for aquaculture","volume":"76","author":"Pankhurst","year":"2010","journal-title":"J. Fish Biol."},{"key":"2021042507020244300_R41","doi-asserted-by":"crossref","first-page":"14552","DOI":"10.1074\/jbc.M800593200","article-title":"Evidence that proline focuses movement of the floppy loop of arylalkylamine N-acetyltransferase (EC 2.3.1.87)","volume":"283","author":"Pavlicek","year":"2008","journal-title":"J. Biol. Chem."},{"key":"2021042507020244300_R42","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1016\/j.dsr2.2006.02.015","article-title":"Climate-dependent evolution of Antarctic ectotherms: an integrative analysis","volume":"53","author":"P\u00f6rtner","year":"2006","journal-title":"Deep Sea Res. Part II Top. Stud. Oceanogr."},{"key":"2021042507020244300_R43","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1007\/s00792-008-0192-4","article-title":"Amino acid contacts in proteins adapted to different temperatures: hydrophobic interactions and surface charges play a key role","volume":"13","author":"Saelensminde","year":"2009","journal-title":"Extremophiles"},{"key":"2021042507020244300_R44","volume-title":"Molecular Cloning: A Laboratory Manual","author":"Sambrook","year":"2001","edition":"3rd edn."},{"key":"2021042507020244300_R45","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1111\/j.1600-079X.2007.00511.x","article-title":"Keeping track of time under ice and snow in a sub-arctic lake: plasma melatonin rhythms in Arctic charr overwintering under natural conditions","volume":"44","author":"Strand","year":"2008","journal-title":"J. Pineal Res."},{"key":"2021042507020244300_R46","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1111\/j.1471-4159.1993.tb03572.x","article-title":"Regulation of melatonin production by pineal photoreceptor cells: role of cyclic nucleotides in the trout (Oncorhynchus mykiss)","volume":"61","author":"Thibault","year":"1993","journal-title":"J. Neurochem."},{"key":"2021042507020244300_R47","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1038\/sj.hdy.6800635","article-title":"Genome evolution and biodiversity in teleost fish","volume":"94","author":"Volff","year":"2005","journal-title":"Heredity"},{"key":"2021042507020244300_R48","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1006\/jmbi.2001.5371","article-title":"X-ray crystallographic studies of serotonin N-acetyltransferase catalysis and inhibition","volume":"317","author":"Wolf","year":"2002","journal-title":"J. Mol. Biol."},{"key":"2021042507020244300_R49","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/0016-6480(92)90122-Z","article-title":"Effects of photoperiod and temperature on rhythmic melatonin secretion from the pineal organ of the white sucker (Catostomus commersoni) in vitro","volume":"86","author":"Zachmann","year":"1992","journal-title":"Gen. Comp. Endocrinol."},{"key":"2021042507020244300_R50","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.ygcen.2004.05.007","article-title":"Duality of serotonin-N-acetyltransferase in the gilthead seabream (Sparus aurata): molecular cloning and characterization of recombinant enzymes","volume":"138","author":"Zilberman-Peled","year":"2004","journal-title":"Gen. Comp. Endocrinol."},{"key":"2021042507020244300_R51","doi-asserted-by":"crossref","first-page":"906","DOI":"10.3390\/md9050906","article-title":"Molecular evolution of multiple arylalkylamine N-acetyltransferase (AANAT) in fish","volume":"9","author":"Zilberman-Peled","year":"2011","journal-title":"Mar. Drugs"}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/216\/10\/1938\/1873021\/1938.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.080960\/2036842\/jeb_080960.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.080960\/2036842\/jeb_080960.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T20:12:51Z","timestamp":1621368771000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/doi\/10.1242\/jeb.080960\/257673\/Unique-arylalkylamine-N-acetyltransferase-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,1,1]]},"references-count":51,"URL":"https:\/\/doi.org\/10.1242\/jeb.080960","relation":{},"ISSN":["1477-9145","0022-0949"],"issn-type":[{"type":"electronic","value":"1477-9145"},{"type":"print","value":"0022-0949"}],"subject":[],"published":{"date-parts":[[2013,1,1]]},"article-number":"jeb.080960"}}