Skip to main content
SpringerLink
Log in

Characterization of melatonin synthesis in the gastrointestinal tract of rainbow trout (Oncorhynchus mykiss): distribution, relation with serotonin, daily rhythms and photoperiod regulation

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Melatonin is synthesized in peripheral locations of vertebrates, including the gastrointestinal tract (GIT). In teleost, information regarding this topic is scarce. Here we studied the presence and synthesis of melatonin at the rainbow trout GIT. Different sections of trout GIT (from esophagus to hindgut) were dissected out and assayed for contents of melatonin, serotonin (5-HT) and its metabolite, 5-hydroxyindole acetic acid, as well as for aanat1, aanat2 and hiomt mRNA abundance. A trout group was pinealectomized to evaluate changes in plasma and gut melatonin content. Finally, the daily profile of melatonin and 5-HT content, and aanat1, aanat2 and hiomt mRNA abundance were analyzed in gut of trout kept under normal lighting, and then under constant darkness. Melatonin was detected in all GIT regions with higher concentrations in the muscular wall than in the mucosa, a similar trend to that of 5-HT. In contrast, transcripts of melatonin synthesis enzymes were more abundant in the mucosa. Pinealectomy did not affect melatonin levels in midgut and hindgut either at day or at night. Additionally, no daily rhythms could be defined for melatonin content in gut tissues but increases during late light phase and at midnight occurred. However, aanat1, aanat2 and hiomt mRNA abundance showed clear daily rhythms with peaks at night. These rhythms remained with a 3-h phase advanced peak in fish exposed to constant darkness. Our results provide clear evidence for a local synthesis of melatonin in trout GIT that might be influenced by the content of 5-HT in the tissue. The process is affected by environmental light cycle and is likely to be under circadian regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson C, Campbell G (1988) Immunohistochemical study of 5-HT-containing neurons in the teleost intestine: relation to the presence of enterochromaffin cells. Cell Tissue Res 254:553–559

    Article  CAS  PubMed  Google Scholar 

  • Bayarri MJ, Rol De Lama MA, Madrid JA, Sánchez-Vázquez FJ (2003) Both pineal and lateral eyes are needed to sustain daily circulating melatonin rhythms in the sea bass. Brain Res 969:175–182

    Article  CAS  PubMed  Google Scholar 

  • Bégay V, Falcón J, Cahill GM, Klein DC, Coon SL (1998) Transcripts encoding two melatonin synthesis enzymes in the teleost pineal organ: circadian regulation in pike and zebrafish, but not in trout. Endocrinology 139:905–912

    PubMed  Google Scholar 

  • Besseau L, Benyassi A, Møller M, Coon SL, Weller JL, Boeuf G, Klein DC, Falcón J (2006) Melatonin pathway: breaking the “high-at-night” rule in trout retina. Exp Eye Res 82:620–627

    Article  CAS  PubMed  Google Scholar 

  • Bubenik GA (1980) Localization of melatonin in the digestive tract of the rat. Effect of maturation, diurnal variation, melatonin treatment and pinealectomy. Hormone Res 12:313–323

    Article  CAS  PubMed  Google Scholar 

  • Bubenik GA (2002) Gastrointestinal melatonin. Localization, function and clinical relevance. Dig Dis Sci 47:2336–2348

    Article  CAS  PubMed  Google Scholar 

  • Bubenik GA, Brown GM (1997) Pinealectomy reduces melatonin levels in the serum but not in the gastrointestinal tract of rats. Biol Signals 6:40–44

    Article  CAS  PubMed  Google Scholar 

  • Bubenik GA, Pang SF (1994) The role of serotonin and melatonin in gastrointestinal physiology: ontogeny, regulation of food intake and mutual serotonin-melatonin feedback. J Pineal Res 16:91–99

    Article  CAS  PubMed  Google Scholar 

  • Bubenik GA, Pang SF (1997) Melatonin levels in the gastrointestinal tissues of fish, amphibians, and a reptile. Gen Comp Endocrinol 106:415–419

    Article  CAS  PubMed  Google Scholar 

  • Bubenik GA, Pang SF, Hacker RR, Smith PS (1996) Melatonin concentrations in serum and tissues of porcine gastrointestinal tract and their relationship to the intake and passage of food. J Pineal Res 21:251–256

    Article  CAS  PubMed  Google Scholar 

  • Bubenik GA, Hacker RR, Brown GM, Baros L (1999) Melatonin concentrations in the luminal fluid, mucosa and muscularis of the bovine and porcine gastrointestinal tract. J Pineal Res 26:56–63

    Article  CAS  PubMed  Google Scholar 

  • Bubenik GA, Pang SF, Cockshut JR, Smith PS, Grovum LW, Friendship RM, Hacker RR (2000) Circadian variation of portal, arterial and venous blood levels of melatonin in pigs and its relationship to food intake and sleep. J Pineal Res 28:9–15

    Article  CAS  PubMed  Google Scholar 

  • Caamaño-Tubío RI, Pérez J, Ferreiro S, Aldegunde M (2007) Peripheral serotonin dynamics in the rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol Part C 145:245–255

    Google Scholar 

  • Ceinos RM, Rabade S, Soengas JL, Miguez JM (2005) Indoleamines and 5-methoxyindoles in trout pineal organ in vivo: daily changes and influence of photoperiod. Gen Comp Endocrinol 144:67–77

    Article  CAS  PubMed  Google Scholar 

  • Ceinos RM, Polakof S, Rodríguez A, Soengas JL, Míguez JM (2008) Food deprivation and refeeding effects on pineal índoles metabolism and melatonin synthesis in the rainbow trout Oncorhynchus mykiss. Gen Comp Endocrinol 156:410–417

    Article  CAS  PubMed  Google Scholar 

  • Chen CQ, Fichna J, Bashashati M, Li YY, Storr M (2011) Distribution, function and physiological role of melatonin in the lower gut. World J Gastroenterol 14:3888–3898

    Article  Google Scholar 

  • Coon SL, Bégay V, Deurloo D, Falcón J, Klein DC (1999) Two arylalkylamine N-acetyltransferase genes mediate melatonin synthesis in fish. J Biol Chem 274:9076–9082

    Article  CAS  PubMed  Google Scholar 

  • Falcón J (1999) Cellular circadian clocks in the pineal. Prog Neurobiol 58:121–162

    Article  PubMed  Google Scholar 

  • Falcón J, Thibault C, Bégay V, Zackmann A, Collin JP (1992) Regulation of the rhythmic melatonin secretion by the fish pineal photoreceptor cells. In: Ali MA (ed) Rhythms in fishes, NATO ASI series A: life sciences, vol 236. Plenum Press, New York, pp 167–198

    Chapter  Google Scholar 

  • Falcón J, Gothilf Y, Coon SL, Boeuf G, Klein DC (2003) Genetic, temporal and developmental differences between melatonin rhythm generating systems in the teleost fish pineal organ and retina. J Neuroendocrinol 15:378–382

    Article  PubMed  Google Scholar 

  • Falcón J, Migaud H, Muñoz-Cueto JA, Carrillo M (2010) Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol 165:469–482

    Article  PubMed  Google Scholar 

  • Fernández-Durán B, Ruibal C, Polakof S, Ceinos RM, Soengas JL, Míguez JM (2007) Evidence for arylalkylamine N-acetyltransferase (AANAT2) expression in rainbow trout peripheral tissues with emphasis in the gastrointestinal tract. Gen Comp Endocrinol 152:289–294

    Article  PubMed  Google Scholar 

  • Gershon MD, Tack J (2007) The serotonin signaling system: from basic understanding to drug development for functional GI disorders. Gastroenterology 132:397–414

    Article  CAS  PubMed  Google Scholar 

  • Gesto M, Tintos A, Soengas JL, Míguez JM (2006) Effects of acute and prolonged naphthalene exposure on brain monoaminergic neurotransmitters in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol C 144:173–183

    Article  Google Scholar 

  • Hardeland R, Pandi-Perumal SR (2005) Melatonin, a potent agent in antioxidative defense: actions as a natural food constituent, gastrointestinal factor, drug and prodrug. Nutr Metabol 2:22

    Article  Google Scholar 

  • Herrero MJ, Martínez FJ, Míguez JM, Madrid JA (2007) Response of plasma and gastrointestinal melatonin, plasma cortisol and activity rhythms of European sea bass (Dicentrarchus labrax) to dietary supplementation with tryptophan and melatonin. J Comp Physiol B 177:319–326

    Article  CAS  PubMed  Google Scholar 

  • Huether G (1993) The contribution of extrapineal sites of melatonin synthesis to circulating melatonin levels in higher vertebrates. Experientia 49:665–670

    Article  CAS  PubMed  Google Scholar 

  • Huether G, Poegeller B, Reimer R, George A (1992) Effect of tryptophan administration on circulating melatonin levels in chicks and rats: evidence for stimulation of melatonin synthesis and release in the gastrointestinal tract. Life Sci 51:945–953

    Article  CAS  PubMed  Google Scholar 

  • Huether G, Messner M, Rodenbeck A, Hardeland R (1998) Effect of continuos melatonin infusions on steady-state plasma melatonin levels in rats under near physiological conditions. J Pineal Res 24:146–151

    Article  CAS  PubMed  Google Scholar 

  • Iigo M, Abe T, Kambayashi S, Oikawa K, Masuda T, Mizusawa K, Kitamura S, Azuma T, Takagi Y, Aida K, Yanagisawa T (2007) Lack of circadian regulation of in vitro melatonin release from the pineal organ of salmonid teleosts. Gen Comp Endocrinol 154:91–97

    Article  CAS  PubMed  Google Scholar 

  • Kezuka H, Iigo M, Furukawa K, Aida K, Hanyu I (1992) Effects of photoperiod, pinealectomy and ophthalmectomy on circulating melatonin rhythms in the goldfish, Carassius auratus. Zool Sci 9:1047–1053

    CAS  Google Scholar 

  • Klein DC (2007) Arylalkylamine N-acetyltransferase: the “timezyme”. J Biol Chem 282:4233–4237

    Article  CAS  PubMed  Google Scholar 

  • Lepage O, Larson ET, Mayer I, Winberg S (2005) Tryptophan affects both gastrointestinal melatonin production and interrenal activity in stressed and nonstressed rainbow trout. J Pineal Res 38:264–271

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • López-Patiño MA, Rodríguez-Illamola A, Gesto M, Soengas JL, Míguez JM (2014) Changes in plasma melatonin levels and pineal organ melatonin synthesis following acclimation of rainbow trout (Oncorhynchys mykiss) to different water salinities. J Exp Biol 214:928–936

    Article  Google Scholar 

  • Migaud H, Davie A, Martínez Chavez CC, Al-Khamees S (2007) Evidence for differential photic regulation of pineal melatonin synthesis in teleosts. J Pineal Res 43:327–335

    Article  CAS  PubMed  Google Scholar 

  • Mizusawa K, Iigo M, Masuda T, Aida K (2000) Photic regulation of arylalkylamine N-acetyltransferase 1 mRNA in trout retina. Neuroreport 9:3473–3477

    Article  Google Scholar 

  • Mukherjeea S, Moniruzzamana M, Maitraa SK (2014a) Daily and seasonal profiles of gut melatonin and their temporal relationship with pineal and serum melatonin in carp Catla catla under natural photo-thermal conditions. Biol Rhythm Res 45:301–315

    Article  Google Scholar 

  • Mukherjeea S, Moniruzzamana M, Maitraa SK (2014b) Impact of artificial lighting conditions on the diurnal profiles of gut melatonin in a surface dwelling carp (Catla catla). Biol Rhythm Res 45:831–848

    Article  Google Scholar 

  • Muñoz JLP, Ceinos RM, Soengas JL, Míguez JM (2009) A simple and sensitive method for determination of melatonin in plasma, bile and intestinal tissues by high performance liquid chromatography with fluorescence detection. J Chromatogr B 877:2173–2177

    Article  Google Scholar 

  • Nisembaum LG, Tinoco AB, Moure AL, Alonso Gómez AL, Delgado MJ, Valenciano AI (2013) Arylalkylamine-N-acetyltransferase (AANAT) acetylates dopamine in the digestive tract of goldfish: a role in intestinal melatonin. Neurochem Int 62:873–880

    Article  CAS  PubMed  Google Scholar 

  • Pévet P, Agez L, Bothorel B, Saboureau M, Gauer F, Laurent V, Masson-Pévet M (2006) Melatonin in the multi-oscillatory mammalian circadian world. Chronobiol Int 23:39–51

    Article  PubMed  Google Scholar 

  • Reiter RJ (1993) The melatonin rhythm: both a clock and a calendar. Experientia 49:654–664

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Vázquez FJ, Iigo M, Madrid JA, Tabata M (2000) Pinealectomy does not affect the entrainment to light nor the generation of the circadian demand-feeding rhythms of rainbow trout. Physiol Behav 69:455–461

    Article  PubMed  Google Scholar 

  • Spiller R (2008) Serotonin and GI clinical disorders. Neuropharmacology 55:1072–1080

    Article  CAS  PubMed  Google Scholar 

  • Tan DX, Manchester LC, Reiter RJ, Qi W, Hanes M, Farley NJ (1999) High physiological levels of melatonin in the bile of mammals. Life Sci 65:2523–2529

    Article  CAS  PubMed  Google Scholar 

  • Van`t Hof TJ, Gwinner E (1999) Influence of pinealectomy and pineal stalk deflection on circadian gastrointestinal tract melatonin rhythms in zebra fish (Taenioppygia guttata). J Biol Rhythms 14:185–189

    Article  CAS  Google Scholar 

  • Velarde E, Alonso-Gómez AL, Azpeleta C, Isorna E, Delgado MJ (2009) Melatonin attenuates the acetylcholine-induced contraction in isolated intestine of a teleost fish. J Comp Physiol B 179:951–959

    Article  CAS  PubMed  Google Scholar 

  • Velarde E, Cerdá-Reverter JM, Alonso-Gómez AL, Sánchez E, Isorna E, Delgado MJ (2010) Melatonin-synthesizing enzymes in pineal, retina, liver, and gut of the goldfish (Carassius auratus): mRNA expression pattern and regulation of daily rhythms by lighting conditions. Chronobiol Int 27:1178–1201

    Article  CAS  PubMed  Google Scholar 

  • Vera LM, De Pedro N, Gómez-Milán E, Delgado MJ, Sánchez-Muros MJ, Madrid JA, Sánchez-Vázquez FJ (2007) Feeding entrainment of locomotor activity rhythms, digestive enzymes and neuroendocrine factor in goldfish. Physiol Behav 90:518–524

    Article  CAS  PubMed  Google Scholar 

  • Vuilleumier R, Boeuf G, Fuentes M, Gehring WJ, Falcón J (2007) Cloning and early expression pattern of two melatonin biosynthesis enzymes in the turbot (Scophthalmus maximus). Eur J Neurosci 25:3047–3057

    Article  PubMed  Google Scholar 

  • Yaga H, Reiter RJ, Richardson BA (1993) Tryptophan loading increase day time serum melatonin in intac and pinealectomized rats. Life Sci 52:1231–1238

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Spanish Ministerio de Economía y Competitividad and European Fund for Regional Development (AGL2013-46448-C3-1-R and FEDER), and by Proyecto FONDECYT 11121498 from Chile Government. The authors are grateful to Marta Conde Sieira for excellent technical assistance.

Author information

Author notes

  1. José L. Muñoz-Pérez

    Present address: Centro I-Mar, Universidad de Los Lagos, Puerto Montt, Chile

  2. Manuel Gesto

    Present address: DTU-AQUA National Institute of Aquatic Resources, Technical University of Denmark, Hirtshals, Denmark

Authors and Affiliations

  1. Laboratorio de Fisioloxía Animal, Departamento de Bioloxía Funcional e Ciencias da Saúde, Facultade de Bioloxía, Universidade de Vigo, 36310, Vigo, Spain

    José L. Muñoz-Pérez, Marcos A. López-Patiño, Rosa Álvarez-Otero, Manuel Gesto, José L. Soengas & Jesús M. Míguez

Authors
  1. José L. Muñoz-Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcos A. López-Patiño
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rosa Álvarez-Otero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manuel Gesto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José L. Soengas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jesús M. Míguez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jesús M. Míguez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest. Funding that supported this study have no role in the study design, data collected or publication of the results. The research included in this study was funded by projects AGL2013-46448-C3-1-R from the Spanish Ministerio de Economía y Competitividad and European Fund for Regional Development (FEDER), and by Proyecto FONDECYT 11121498 from Chile Government. JLMP was recipient of a doctoral fellowship from CONICYT (Chile Government) for a part of this study. MG was recipient of a post-doctoral fellowship from Xunta de Galicia (Plan I2C).

Ethical standards

The experimental procedures and animal manipulation were performed according to the European Union Council (2010/63/EU), and the Spanish Government (RD 55/2013) legal requirements. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution and previously approved by the Comité de Etica de la Universidad de Vigo.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muñoz-Pérez, J.L., López-Patiño, M.A., Álvarez-Otero, R. et al. Characterization of melatonin synthesis in the gastrointestinal tract of rainbow trout (Oncorhynchus mykiss): distribution, relation with serotonin, daily rhythms and photoperiod regulation. J Comp Physiol B 186, 471–484 (2016). https://doi.org/10.1007/s00360-016-0966-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-016-0966-4

Keywords

Search

Navigation