Daily Rhythmic Expression Patterns of Melatonin Bio-synthesizing Genes in Zebrafish (Danio rerio) Testis in Response to Altered Feeding Condition

Jump To References Section

Authors

  • Sijagurumayum Dharmajyoti Devi
     Biological Rhythm Laboratory, Animal Resources Programme, Institute of Bioresources and Sustainable Development, Department of Biotechnology, Government of India, Takyelpat, Imphal - 795 001, Manipur ,IN
  • Gopinath Mondal
     Biological Rhythm Laboratory, Animal Resources Programme, Institute of Bioresources and Sustainable Development, Department of Biotechnology, Government of India, Takyelpat, Imphal - 795 001, Manipur ,IN
  • Zeeshan Ahmad Khan
     Biological Rhythm Laboratory, Animal Resources Programme, Institute of Bioresources and Sustainable Development, Department of Biotechnology, Government of India, Takyelpat, Imphal - 795 001, Manipur ,IN
  • Rajendra K. Labala
     Biological Rhythm Laboratory, Animal Resources Programme, Institute of Bioresources and Sustainable Development, Department of Biotechnology, Government of India, Takyelpat, Imphal - 795 001, Manipur ,IN
  • Hridip Kumar Sarma
     Department of Biotechnology, Gauhati University, Guwahati - 781 014, Assam ,IN
  • Asamanja Chattoraj
     Biological Rhythm Laboratory, Department of Animal Science, Kazi Nazrul University, Paschim Bardhaman, Asansol - 713 340, West Bengal ,IN

DOI:

https://doi.org/10.18311/jer/2020/27222

Keywords:

Circadian Rhythm, Feeding, Melatonin, Melatonin Biosynthesis, Testis

Abstract

The alternation of light (L) and darkness (D) cycle is the most important zeitgeber ("time giver”) of the circadian system. Still, feeding time also acts as a potent synchronizer of the teleost circadian system. In fish, the impact of the altered photoperiodic condition is known, but the impact of altered feeding cycles in the daily rhythm of fish circadian system is largely unknown. The objective of this work was to explore how 12 hr shift in feeding time alters expression of genes concerned with melatonin synthesizing enzymes in zebrafish testis tissue. In this study, zebrafish maintained under a 12 hr light-12 hr darkness were fed at light phase (ZT03 and ZT10) in normal feeding (NF) group and another one was the altered feeding group (AF) fed at dark phase (ZT15 and 22) for 30 days. Daily rhythms of expression of genes concerned with melatonin synthesizing enzymes and circulating melatonin level were studied. The 12 hr shift in scheduled feeding induced a phase delay of 4-5 hr in the acrophases in the case of aanat2, 10-11 hr for asmt and 4 hr for aanat1 but a slight shift seems to exist in case of tph1. Serum melatonin levels showed a significant daily rhythm in both condition but displayed phase delay in AF condition. Rhythmic expression of aanat2 and peak at midnight corresponds with the high concentration of melatonin during the night. Melatonin is a multi-potent molecule; the change in the rhythmic expression of its bio-synthesizing enzyme genes through altered feeding time may lead to desynchronization in the physiology.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Downloads

Published

2021-04-16

How to Cite

Dharmajyoti Devi, S., Mondal, G., Ahmad Khan, Z., Labala, R. K., Kumar Sarma, H., & Chattoraj, A. (2021). Daily Rhythmic Expression Patterns of Melatonin Bio-synthesizing Genes in Zebrafish (<i>Danio rerio</i>) Testis in Response to Altered Feeding Condition. Journal of Endocrinology and Reproduction, 24(1), 31–41. https://doi.org/10.18311/jer/2020/27222

Issue

Volume 24, Issue 1, June 2020

Section

Original Research
Crossref
Scopus
Google Scholar
Europe PMC

 

References

Rensing L, Ruoff P. Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular bases. Chronobiol Int. 2002; 19(5):807-864. https://doi.org/10.1081/cbi-120014569. PMid: 12405549.

Stephan FK. The "other” circadian system: food as a Zeitgeber. J Biol Rhythms. 2002; 17(4):284-292. https://doi.org/10.1177/074873040201700402. PMid: 12164245.

Mistlberger RE. Circadian food-anticipatory activity: Formal models and physiological mechanisms. Neurosci Biobehav Rev. 1994; 18(2):171-195. https://doi.org/10.1016/0149-7634(94)90023-x. PMid: 8058212.

Tessmar"Raible K, Raible F, Arboleda E. Another place, another timer: marine species and the rhythms of life. Bioessays. 2011; 33(3):165-172. https://doi.org/10.1002/ bies.201000096. PMid: 21254149.

Boulos Z, Terman, M. Food availability and daily biological rhythms. Neurosci Biobehav Rev. 4(2):119-131. https://doi.org/10.1016/0149-7634(80)90010-x. PMid: 6106914.

Boujard T, Leatherland JF. Circadian rhythms and feeding time in fishes. Env Biol Fish. 1992; 35(2):109-131. https:// doi.org/10.1007/bf00002186.

Escobar C, Dí­az-Muñoz M, Encinas F, Aguilar-Roblero R. Persistence of metabolic rhythmicity during fasting and its entrainment by restricted feeding schedules in rats. Am J Physiol. 1998; 274(5):R1309-R1316. https://doi.org/10.1152/ajpregu.1998.274.5.R1309. PMid: 9644044.

Nisembaum LG, Velarde E, Tinoco AB, Azpeleta C, de Pedro N, Alonso-Gomez AL, Delgado MJ, Isorna E. Lightdark cycle and feeding time differentially entrains the gut molecular clock of the goldfish (Carassius auratus). Chronobiol Int. 2012; 29(6):665-673. https://doi.org/10.31 09/07420528.2012.686947. PMid: 22734567.

Vera LM, De Pedro N, Gómez-Milán E, Delgado MJ, Sánchez-Muros MJ, Madrid JA, Sánchez-Vázquez FJ. Feeding entrainment of locomotor activity rhythms, digestive enzymes and neuroendocrine factors in goldfish. Physiol Behav. 2007; 90(2-3):518-524. https://doi.org/10.1016/j.physbeh.2006.10.017. PMid: 17196229.

Chen WM, Naruse M, Tabata M. Circadian rhythms and individual variability of self-feeding activity in groups of rainbow trout Oncorhynchus mykiss (Walbaum). Aquacult Res. 2002; 33(7):491-500. https://doi.org/10.1046/j.13652109.2002.00734.x.

Sánchez-Vázquez FJ, Madrid JA. Feeding anticipatory activity. In: Houlihan D, Boujard T, Jobling M (Eds) Food Intake in Fish. 2001; 216-232. Blackwell Science Publisher. https://doi.org/10.1002/9780470999516.ch9.

Hoskins LJ, Volkoff H. The comparative endocrinology of feeding in fish: Insights and challenges. Gen Comp Endocrinol. 2012; 176(3):327-335. https://doi.org/10.1016/j.ygcen.2011.12.025. PMid: 22226758.

Pinillos M, De Pedro N, Alonso-Gómez A, Alonso-Bedate, Delgad MJ. Physiol Behav. 2001; 72(5):629-34. https://doi.org/10.1016/s0031-9384(00)00399-1 PMid: 11336993.

Rubio V, Sanchez"Vazquez F, Madrid JA. Oral administration of melatonin reduces food intake and modifies macronutrient selection in European sea bass (Dicentrarchus labrax, L.). J Pineal Res. 2004; 37(1):42-47. https://doi.org/10.1111/j.1600-079X.2004.00134.x PMid: 15230867.

Welker H, Vollrath L. The effects of a number of short-term exogenous stimuli on pineal serotonin-N-acetyltransferase activity in rats. J Neural Transm. 1984; 59(1):69-80. https://doi.org/10.1007/BF01249879. PMid: 6371190.

Khan ZA, Yumnamcha T, Rajiv C, Devi HS, Mondal G, Devi SD, Bharali R, Chattoraj A. Melatonin biosynthesizing enzyme genes and clock genes in ovary and whole brain of zebrafish (Danio rerio): Differential expression and a possible interplay. Gen Comp Endocrinol. 2016; 233:1631. https://doi.org/10.1016/j.ygcen.2016.05.014 PMid: 27179881.

Rajiv C, Sanjita Devi H, Mondal G, Devi SD, Khan ZA, Yumnamcha T, Bharali R, Chattoraj A. Cloning, phylogenetic analysis and tissue distribution of melatonin bio-synthesizing enzyme genes (Tph1, Aanat1, Aanat2 and Hiomt) in a tropical carp, Catlacatla. Biol Rhythm Res. 2016; 48(3):371-386. https://doi.org/10.1080/09291016.20 16.1263019.

Chattoraj A, Liu T, Zhang LS, Huang Z, Borjigin J. Melatonin formation in mammals: In vivo perspectives. Rev Endocr Metab Disord. 2009; 10(4):237-243. https:// doi.org/10.1007/s11154-009-9125-5. PMid: 20024626.

Falcon J, Besseau L, Sauzet S, Boeuf G. Melatonin effects on the hypothalamo-pituitary axis in fish. Trends Endocrinol Metab. 2007; 18(2):81-88. https://doi.org/10.1016/j.tem.2007.01.002. PMid: 17267239.

Lerner AB, Case JD, Takahashi Y, Lee TH, Mori W. Isolation of melatonin, the pineal gland factor that lightens melanocytes1. J Am Chem Soc. 1958; 80(10):2587-2587. https://doi.org/10.1021/ja01543a060.

Falcon J, Gothilf Y, Coon SL, Boeuf G, Klein DC. Genetic, temporal and developmental differences between melatonin rhythm generating systems in the teleost fish pineal organ and retina. J Neuroendocrinol. 2003; 15(4):378-382. https://doi.org/10.1046/j.1365-2826.2003.00993.x. PMid: 12622837.

Iuvone PM, Tosini G, Pozdeyev N, Haque R, Klein DC, Chaurasia SS. Circadian clocks, clock networks, arylalkylamine N-acetyltransferase, and melatonin in the retina. Prog Retin Eye Res. 2005; 24(4):433-456. https://doi.org/10.1016/j.preteyeres.2005.01.003 PMid: 15845344.

Klein DC. Arylalkylamine N-acetyltransferase: "the Timezyme”. J Biol Chem. 2007; 282(7):4233-4237. https://doi.org/10.1074/jbc.R600036200. PMid: 17164235.

Mukherjee S, Maitra SK. Effects of starvation, re-feeding and timing of food supply on daily rhythm features of gut melatonin in carp (Catla catla). Chronobiol Int. 2015; 32(9):1264-1277. https://doi.org/10.3109/07420528.2015.1 087020. PMid: 26513010.

Devi HS, Rajiv C, Mondal G, Khan ZA, Devi SD, Yumnamcha T, Bharali R, Chattoraj A. Melatonin biosynthesizing enzyme genes (Tph1, Aanat1, Aanat2, and Hiomt) and their temporal pattern of expression in brain and gut of a tropical carp in natural environmental conditions. Cogent Biology. 2016; 2(1):1230337. https://doi.org/10.1080/23312025.2016.1230337.

Yumnamcha T, Khan ZA, Rajiv C, Devi SD, Mondal G, Sanjita Devi H, Bharali R, Chattoraj A. Interaction of melatonin and gonadotropin-inhibitory hormone on the zebrafish brain-pituitary reproductive axis. 2017; 84(5):389-400. https://doi.org/10.1002/mrd.22795. PMid: 28295807.

González-Arto M, Aguilar D, Gaspar-Torrubia E, Gallego M, Carvajal-Serna M, Herrera-Marcos LV, Serrano-Blesa E, Hamilton TR d S, Pérez-Pé R, Muiño-Blanco, Pérez Cebrián J A, Casao A. Melatonin MT1 and MT2 receptors in the ram reproductive tract. Int. J. Mol. Sci. 2017; 18(3):662. https://doi.org/10.3390/ijms18030662. PMid: 28335493 PMCid: PMC5372674.

Izzo G, Francesco A, Ferrara D, Campitiello MR, Serino I, Minucci S, d'Istria M. Expression of melatonin (MT1, MT2) and melatonin-related receptors in the adult rat testes and during development. Zygote. 2010; 18(3):257-264. https://doi.org/10.1017/S0967199409990293. PMid: 20109269.

Tabecka-Lonczynska A, Mytych J, Solek P, Kulpa M, Koziorowski M. New insight on the role of melatonin receptors in reproductive processes of seasonal breeders on the example of mature male European bison (Bison bonasus, Linnaeus 1758). J Photochem Photobiol. 2017; 173:84-91. https://doi.org/10.1016/j.jphotobiol.2017.05.026. PMid: 28570908.

Challet E, Pevet P, Vivien-Roels B, Malan A. Phaseadvanced daily rhythms of melatonin, body temperature, and locomotor activity in food-restricted rats fed during daytime. J Biol Rhythms. 1997; 12(1):65-79. https://doi.org/10.1177/074873049701200108. PMid: 9104691.

Ceinos RM, Polakof S, Illamola AR, Soengas JL, Mí­guez JM. Food deprivation and refeeding effects on pineal indoles metabolism and melatonin synthesis in the rainbow trout Oncorhynchus mykiss. Gen Comp Endocrinol. 2008; 156(2):410-417. https://doi.org/10.1016/j.ygcen.2008.01.003. PMid: 18275959.

Fernandez-Duran B, Ruibal C, Polakof S, Ceinos RM, Soengas JL, Miguez JM. Evidence for arylalkylamine N-acetyltransferase (AANAT2) expression in rainbow trout peripheral tissues with emphasis in the gastrointestinal tract. Gen Comp Endocrinol. 2007; 152(2-3):289-94. https://doi.org/10.1016/j.ygcen.2006.12.008 PMid: 17292900.

Sánchez-Vázquez F, Madrid J, Zamora S, Iigo M, Tabata M. Demand feeding and locomotor circadian rhythms in the goldfish, Carassius auratus: dual and independent phasing. Physiol Behav. 1996; 60(2): 665-74. https://doi.org/10.1016/s0031-9384(96)80046-1. PMid: 8840933.

Bolliet V, Aranda A, Boujard. Demand-feeding rhythm in rainbow trout and European catfish: synchronisation by photoperiod and food availability. Physiol Behav. 2001; 73(4):625-633. https://doi.org/10.1016/s00319384(01)00505-4. PMid: 11495668.

Damiola F, Le Minh N, Preitner N, Kornmann B, FleuryOlela F, Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000; 14(23):2950-2961. https://doi.org/10.1101/gad.183500. PMid: 11114885.

Stokkan K A, Yamazaki S, Tei H, Sakaki Y, Menaker M. Entrainment of the circadian clock in the liver by feeding. Science. 2001; 291(5503):490-493. https://doi.org/10.1126/ science.291.5503.490. PMid: 11161204.

Reed B, Jennings M. Guidance on the housing and care of zebrafish, Danio rerio: Research Animals Department, Science Group, RSPCA. 2011. http://www.rspca.org.uk/home.

Westerfield M. The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio). Eugene, OR: University of Oregon Press 2000; 4th ed. https://zfin.org/zf_info/zfbook/zfbk.html.

Portaluppi F, Smolensky MH, Touitou Y. Ethics and methods for biological rhythm research on animals and human beings. Chronobiol Int. 2010; 27(9-10):1911-1929. https://doi.org/10.3109/07420528.2010.516381. PMid: 20969531.

Costa LS, Serrano I, Sánchez-Vázquez FJ, López-Olmeda JF. Circadian rhythms of clock gene expression in Nile tilapia (Oreochromis niloticus) central and peripheral tissues: influence of different lighting and feeding conditions. J Comp Physiol B. 2016; 186:775-785. https://doi.org/10.1007/s00360-016-0989-x. PMid: 27085855.

Vera L M, Negrini P, Zagatti C, Frigato E, SánchezVázquez FJ, Bertolucci C. Light and feeding entrainment of the molecular circadian clock in a marine teleost (Sparus aurata). Chronobiol Int. 2013; 30(5):649-661. https://doi.org/10.3109/07420528.2013.775143 PMid: 23688119.

Chattoraj A, Bhattacharyya S, Basu D, Bhattacharya S, Bhattacharya S, Maitra SK. Melatonin accelerates maturation inducing hormone (MIH): Induced oocyte maturation in carps. Gen Comp Endocrinol. 2005; 140(3):145155. https://doi.org/10.1016/j.ygcen.2004.10.013. PMid: 15639142.

Novak CM, Jiang X, Wang C, Teske JA, Kotz CM, Levine JA. Caloric restriction and physical activity in zebrafish (Danio rerio). Neurosci Lett. 2005; 383(1-2):99-104. https://doi.org/10.1016/j.neulet.2005.03.048. PMid: 15936519.

Amaral IP, Johnston IA. Circadian expression of clock and putative clock-controlled genes in skeletal muscle of the zebrafish. Integrative Physiology C. 2012; 302(1):R193-R206. https://doi.org/10.1152/ajpregu.00367.2011. PMid: 22031781.

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25(4):402408. https://doi.org/10.1006/meth.2001.1262. PMid: 11846609.

Tang R, Dodd A, Lai D, McNabb WC, Love DR. Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin (Shanghai). 2007; 39(5):384-390. https://doi.org/10.1111/j.1745-7270.2007.00283.x PMid: 17492136. PMCid: PMC7110012.

Khan ZA, Labala RK, Yumnamcha T, Devi SD, Mondal G, Sanjita Devi H, Rajiv C, Bharali R, Chattoraj A. Artificial Light at Night (ALAN), an alarm to ovarian physiology: A study of possible chronodisruption on zebrafish (Danio rerio). Sci Total Environ. 2018; 628-629:1407-1421. https://doi.org/10.1016/j.scitotenv.2018.02.101. PMid: 30045561.

Babaei F, Ramalingam R, Tavendale A, Liang Y, Yan LSK, Ajuh P, Cheng SH, Lam. Novel blood collection method allows plasma proteome analysis from single zebrafish. J Proteome Res. 2013; 12(4):1580-1590. https://doi:10.1021/ pr3009226 PMid: 23413775.

Refinetti R, Cornélissen G, Halberg F. Procedures for numerical analysis of circadian rhythms. Biol Rhythm Res. 2007; 38(4):275-325. https://doi.org/10.1080/09291010600903692. PMid: 23710111 PMCid: PMC3663600.

Nelson W, Tong YL, LEE JK, Halberg F. Methods for cosinor-rhythmometry. Chronobiologia. 1979; 6(4):305323. PMid: 548245.

Aranda A, Madrid J, Sánchez-Vázquez. Influence of light on feeding anticipatory activity in goldfish. J Biol Rhythms. 2001; 16(1):50-57. https://doi.org/10.1177/074873040101600106. PMid: 11220779.

Lopez-Olmeda JF, Montoya A, Oliveira C, Sanchez-Vazquez FJ. Synchronization to light and restricted-feeding schedules of behavioral and humoral daily rhythms in gilthead sea bream (Sparus aurata). Chronobiol Int. 2009; 26(7):13891408. https://doi.org/10.3109/07420520903421922. PMid: 19916838.

Refinetti R. Comparison of light, food, and temperature as environmental synchronizers of the circadian rhythm of activity in mice. J Physiol Sci. 2015; 65(4):359-366. https:// doi.org/10.1007/s12576-015-0374-7. PMid: 25800223.

Feliciano A, Vivas Y, de Pedro N, Delgado MJ, Velarde E, Isorna E. Feeding time synchronizes clock gene rhythmic expression in brain and liver of goldfish (Carassius auratus). J Biol Rhythms. 2011; 26(1):24-33. https://doi:10.1177/0748730410388600. PMid: 21252363.

Chik C, Ho A, Brown GM. Effect of food restriction on 24-h serum and pineal melatonin content in male rats. Acta Endocrinol (Copenh). 1987; 115(4):507-513. https://doi.org/10.1530/acta.0.1150507. PMid: 3630542.

Nikki J, Pirhonen J, Jobling M, Karjalainen J. Compensatory growth in juvenile rainbow trout, Oncorhynchus mykiss (Walbaum), held individually. Aquaculture. 2004; 235(1-4):285-296. https://doi.org/10.1016/j.aquaculture.2003.10.017.

Falcon J, Migaud H, Munoz-Cueto JA, Carrillo M. Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol. 2010; 165(3):469-482. https://doi.org/10.1016/j.ygcen.2009.04.026. PMid: 19409900.

Most read articles by the same author(s)