Short-Term In Vivo Melatonin Activates Thyroid Axis but Deactivates Interrenal Axis in Climbing Perch (Anabas testudineus Bloch)


Affiliations

  • University of Kerala, Department of Zoology, Thiruvananthapuram, Kerala, 695581, India
  • University of Kerala, Inter-University Centre for Evolutionary and Integrative Biology (iCEIB), Thiruvananthapuram, Kerala, 695581, India

Abstract

As a potent regulator of seasonal and circadian rhythms, melatonin is involved in many neuroendocrine functions in vertebrates including fishes. However, the interactive action of melatonin on thyroid and interrenal axes, metabolite homeostasis and ion status is less addressed in fishes. We thus analyze the plasma thyroxine (T4), triiodothyronine (T3) and cortisol levels and metabolite status and Na+ and K+ status in osmoregulatory tissues after short-term of 30 min in vivo exposure of melatonin (0, 0.25, 2.5, 25 ng g-1) in climbing perch (Anabas testudineus Bloch). A rise in plasma T4 occurred after 30 min of melatonin treatment, indicating activation of thyroid axis. On the contrary, deactivation of hypothalamo-pituitary-interenal (HPI) axis occurred due to fall in cortisol level along with decrease in plasma T3 in the melatonin-treated fish. Significant dose-dependent increase in plasma glucose and urea were found in melatonin-treated fish. Similarly, increased plasma [Na+] and [K+] contents occurred in gill tissues but plasma [Na+] and [K+] levels remained unaffected after melatonin treatment. In kidney, melatonin treatment augmented [K+] but decreased [Na+] content, emphasizing a differential cation handling by melatonin. Overall, these results indicate that melatonin exerts a rapid activation of thyroid axis, but deactivates interenal axis while promoting the release of glucose and urea and tissue Na+/K+ ion levels in freshwater climbing perch.

Keywords

Cortisol, Fish, Interrenal Axis, Melatonin, Metabolites, Tissue Ions, Thyroid Axis, Thyroid Hormone

Full Text:

References

Falcón J, Besseau L, Sauzet S, Boeuf G. Melatonin effects on the hypothalamo-pituitary axis in fish. Trends Endocrinol Metab. 2007; 18:81-8. https://doi.org/10.1016/j.tem.2007.01.002

Kulczykowska E. A review of the multifunctional hormone melatonin and a new hypothesis involving osmoregulation. Rev Fish Biol Fish. 2002; 11:321-30. https://doi. org/10.1023/A:1021348822635

Kulczykowska E, Kalamarz H, Warne JM, Balment RJ. Day-night specific binding of 2-[125I] iodomelatonin and melatonin content in gill, small intestine and kidney of three fish species. J Comp Physiol B. 2006; 176:277-85. https://doi.org/10.1007/s00360-005-0049-4

ZhdanovaI V, Wang SY, Leclair OU, Danilova NP. Melatonin promotes sleep-like state in zebrafish. Brain Res. 2001; 903:263-8. https://doi.org/10.1016/S0006-8993(01)02444-1

Danilova N, Krupnik VE, Sugden D, Zhdanova IV. Melatonin stimulates cell proliferation in zebrafish embryo and accelerates its development. FASEB J. 2004; 18:751-3. https://doi.org/10.1096/fj.03-0544fje

Falcón J, Besseau L, Fazzari D, Attia J, Gaildrat P, Beauchaud M, Boeuf G. Melatonin modulates secretion of growth hormone and prolactin by trout pituitary glands and cells in culture. Endocrinology. 2003; 144:4648-58. https://doi.org/10.1210/en.2003-0707

Amano M, Iigo M, Ikuta K, Kitamura S, Okuzawa K, Yamada H, Yamamori K. Disturbance of plasma melatonin profile by high dose melatonin administration inhibits testicular maturation of precocious male masu salmon. Zool Sci. 2004; 21:79-85. https://doi.org/10.2108/0289- 0003(2004)21[79:DOPMPB]2.0.CO;2

Sébert ME, Legros C, Weltzien FA, Malpaux B, Chemineau P, Dufour S. Melatonin activates brain dopaminergic systems in the eel with an inhibitory impact on reproductive function. J Neuroendocrinol. 2008; 20:917-29. https://doi.org/10.1111/j.1365-2826.2008.01744.x

Stankov B, Fraschinin F, Reiter RJ. The melatonin receptor: distribution, biochemistry, and pharmacology. In: You HS, Reiter RJ. (Eds.), Melatonin: Biosynthesis, Physiological Effects, and Clinical Applications. CRC Press, Boca Raton. 1993; pp. 155-86.

Bromage N, Porter M, Randall C. The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture. 2001; 197:63-98. https://doi.org/10.1016/ S0044-8486(01)00583-X

Cahill GM. Clock mechanisms in zebrafish. Cell Tissue Res. 2002; 309:27-34. https://doi.org/10.1007/s00441-002- 0570-7

Wendelaar Bonga SE. The stress response in fish. Physiol Rev. 1997; 77:591-625. https://doi.org/10.1152/physrev. 1997.77.3.591

Peter VS, Peter MCS. The interruption of thyroid and interrenal and the inter-hormonal interference in fish: does it promote physiologic adaptation or maladaptation? Gen Comp Endocrinol. 2011; 174, 249-258. https://doi.org/10.1016/j.ygcen.2011.09.018

Simi S, Peter VS, Peter MCS. Zymosan-induced immune challenge modifies the stress response of hypoxic air-breathing fish (Anabas testudineus Bloch): Evidence for reversed patterns of cortisol and thyroid hormone interaction, differential ion transporter functions and non-specific immune response. Gen Comp Endocrinol. 2017; 251:94-108. https://doi.org/10.1016/j.ygcen.2016.11.009

Saito D, Shi Q, Ando H, Urano A. Attenuation of diurnal rhythms in plasma levels of melatonin and cortisol, and hypothalamic contents of vasotocin and isotocin mRNAs in pre-spawning chum salmon. Gen Comp Endocrinol. 2004; 137:62-8. https://doi.org/10.1016/j.ygcen.2004.02.010

Ebbesson LOE, Björnsson BT, Ekström P, Stefansson SO. Daily endocrine profiles in parr and smolt Atlantic salmon. Comp Biochem Physiol A. 2008; 151:698-704. https://doi. org/10.1016/j.cbpa.2008.08.017

Pavlidis M, Greenwood L, Paalavuo M, Mölsä H, Laitinen JT. The effect of photoperiod on diel rhythms in serum melatonin, cortisol, glucose, and electrolytes in the common dentex, Dentex dentex. Gen Comp Endocrinol. 1999; 113:240-50. https://doi.org/10.1006/gcen.1998.7190

Peter MCS. The role of thyroid hormones in stress response of fish. Gen Comp Endocrinol. 2011; 172:198-210. https:// doi.org/10.1016/j.ygcen.2011.02.023

Peter VS, Joshua EK, Wendelaar Bonga SE, Peter MCS. Metabolic and thyroidal response in air-breathing perch (Anabas testudineus) to water-borne kerosene. Gen Comp Endocrinol. 2007; 152:198-205. https://doi.org/10.1016/j. ygcen.2007.05.015

Gupta BBP, Premabati Y. Differential effects of melatonin on plasma levels of thyroxine and triiodothyronine levels in the air breathing fish Clarias gariepinus during breeding and quiescent periods. Gen Comp Endocrinol. 2002; 129:146- 51. https://doi.org/10.1016/S0016-6480(02)00527-0

Samejima M, Shavali S, Tamotsu S, Uchida K, Morita Y, Fukada A. Light and temperature-dependence of the lampreys, Lampetra japonica. Jpn J Physiol. 2000; 50:437-42. https://doi.org/10.2170/jjphysiol.50.437

Ozturk G, Coskun S, Erbas D, Hasanoglu E. The effect of melatonin on liver superoxide dismutase activity, serum nitrate and thyroid hormone levels. Jpn J Physiol. 2000; 50: 149-53. https://doi.org/10.2170/jjphysiol.50.149

Sjöblom M. The duodenal mucosal bicarbonate secretion. Ups J Med Sci. 2005; 110:115-50. https://doi. org/10.3109/2000-1967-076

Conde-Sieira M, Libran-Perez M, Lopez Patino MA, Soengas JL, Miguez JM. Melatonin treatment alters glucosensing capacity and mRNA expression levels of peptides related to food intake control in rainbow trout hypothalamus. Gen Comp Endocrinol. 2012; 178:131-8. https://doi.org/10.1016/j.ygcen.2012.04.011

De Pedro N, Martínez-Ãlvarez R, Delgado MJ. Melatonin reduces body weight in goldfish (Carassius auratus): effects on metabolic resources and some feeding regulators. J Pineal Res. 2008; 45:32-9. https://doi.org/10.1111/j.1600-079X.2007.00553.x

Rubio VC, Sánchez-Vázquez FJ, 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: 42-7. https://doi.org/10.1111/j.1600-079X.2004.00134.x

Peter MCS, Leji J, Peter VS. Ambient salinity modifies the action of triiodothyronine in the air-breathing fish Anabas testudineus Bloch: effects on mitochondria-rich cell distribution, osmotic and metabolic regulations. Gen Comp Endocrinol. 2011; 171:225-31. https://doi.org/10.1016/j. ygcen.2011.01.013

Peter MCS, Rejitha V. Interactive effects of ambient acidity and salinity on thyroid function during acidic and post-acidic acclimation of air-breathing fish (Anabas testudineus Bloch). Gen Comp Endocrinol. 2011; 174:175-83. https://doi.org/10.1016/j.ygcen.2011.08.018

Peter MCS, Lock RAC, WendelaarBonga SE. Evidence for an osmoregulatory role of thyroid hormones in the freshwater Mozambique tilapia, Oreochromis mossambicus Peters. Gen Comp Endocrinol. 2000; 120:157-67. https:// doi.org/10.1006/gcen.2000.7542

Peter MCS. Thyroid hormones and hydromineral regulation during stress in fish. D.Sc. thesis, Radboud University Nijmegen, The Netherlands, 2007.

Moore CB, Siopes TD. Melatonin enhances cellular and humoral immune responses in the Japanese quail (Coturnix coturnix japonica) via an opiatergic mechanism. Gen Comp Endocrinol. 2003; 131:258-63. https://doi.org/10.1016/ S0016-6480(03)00011-X

Iigo M, Fujimoto Y, Gunji-Suzuki M, Yokosuka M, Hara M, Ohtani-Kaneko R, Tabata M, Aida K, Hirata K. Circadian rhythm of melatonin release from the photoreceptive pineal organ of a teleost, ayu (Plecoglossus altivelis) in flow-through culture. J Neuroendocrinol. 2004; 16:45-51. https://doi.org/10.1111/j.1365-2826.2004.01132.x

Macchi MM, Bruce JN. Human pineal physiology and functional significance of melatonin. Front Neuroendocrinol. 2004; 25:233-42. https://doi.org/10.1016/j.yfrne.2004.08.001

Azpeleta C, Martínez-Alvarez RM, Delgado MJ, Isorna E, De Pedro N. Melatonin reduces locomotor activity and circulating cortisol in goldfish, Horm Behav. 2010; 57:323-9. https://doi.org/10.1016/j.yhbeh.2010.01.001

Herrero MJ, Martínez FJ, Míguez JM, Madrid JA. 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. 2007; 177:319-26. https://doi.org/10.1007/s00360-006-0131-6

Falcón J. Nocturnal melatonin synthesis: How to stop it. Endocrinology. 2007; 148:1473-4. https://doi.org/10.1210/ en.2007-0076

Hazlerigg DG. What is the role of melatonin within the anterior pituitary? J Endocrinol. 2001; 170:493-501. https:// doi.org/10.1677/joe.0.1700493

Carrillo-Vico A, Guerrero, JM, Lardone PJ, Reiter RJ. A review of the multiple actions of melatonin on the immune system. Endocrine. 2005; 27:189-200. https://doi. org/10.1385/ENDO:27:2:189

Zimecki M. The lunar cycle: Effects on human and animal behavior and physiology. Postepy Hig Med Dosw. 2006; 60:1-7.

Appa-Rao NV, Raza B, Prasad JK, Razi SS, Gottardo L, Ahmand MF. Melatonin decreases glucorticoid blood concentration in the rat and palm squirrel, acting directly on the adrenal gland. Biomed Res. 2001; 22:115-17. https://doi.org/10.2220/biomedres.22.115

Saito S, Tachibana T, Choi YH, Denbow DM, Furuse M. ICV melatonin reduces stress responses in neonatal chicks. Behav Brain Res. 2005; 165: 197- 203. https://doi. org/10.1016/j.bbr.2005.06.045

Arjona F, Vargas-Chacoff L, Rio MPMD, Flik G. Effects of cortisol and thyroid hormone on peripheral outer ring deiodination and osmoregulatory parameters in the Senegalese sole (Solea senegalensis). J Endocrinol. 2011; 208:323-30. https://doi.org/10.1530/JOE-10-0416

Puig-Domingo M, Webb SM, Serrano J. Brief report: melatonin-related hypogonadotropic hypogonadism. N Engl J Med. 1992; 327:1356-9. https://doi.org/10.1056/NEJM199211053271905

Power DM., Llwellyn L, Faustino M, Nowell MA, Th. Bjornsson B, Einarsdottir IE, Canario AVM, Sweeney GE. Thyroid hormones in growth and development of fish. Comp Biochem. Physiol. 2001; 130:447-59. https://doi.org/10.1016/S1532-0456(01)00271-X

Leloup J, Lebel JM. Triiodothyronine is necessary for the action of growth hormone in acclimation to seawater of brown (Salmotrutta) and rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem. 1993; 11:165-73. https:// doi.org/10.1007/BF00004563

Klaren PHM, Geven EJW, Flik G. The involvement of the thyroid gland in teleost osmoregulation. In: Baldisserotto B, Mancera JM, Kapoor BG(Eds) Fish Osmoregulation, Science Publishers, Enfield (NH). 2007; pp 35-65. https:// doi.org/10.1201/b10994-3

Peter MCS, Joshua EK, Rejitha V, Peter VS. Thyroid hormone modifies the metabolic response of air-breathing perch (Anabas testudineus Bloch) to nimbecidine exposure. J Endocrinol Reprod. 2009; 13:27-36.

Borges-Silva CN, Takada J, Alonso-Vale MIC, Peres SB, Fonseca-Alaniz MH, Andreotti S. Pinealectomy reduces hepatic and muscular glycogen content and attenuates aerobic power adaptability in trained rats. J Pineal Res. 2007; 43:96-103. https://doi.org/10.1111/j.1600- 079X.2007.00450.x

Polakof S, Míguez JM, Soengas JL. Changes in food intake and glucosensing function of hypothalamus and hindbrain in rainbow trout subjected to hyperglycemic or hypoglycemic conditions. J Comp Physiol A. 2008; 194:829-39. https://doi.org/10.1007/s00359-008-0354-y

Peschke E, Stumpf I, Bazwinsky I, Litvak L, Dralle H, Mühlbauer E. Melatonin and type 2 diabetes - a possible link. J Pineal Res. 2007; 42:350-8. https://doi.org/10.1111/ j.1600-079X.2007.00426.x

Peschke E, Mühlbauer E. New evidence for a role of melatonin in glucose regulation. Best Practice Res Clin Endocrinol Metab. 2010; 24:829-41. https://doi.org/10.1016/j. beem.2010.09.001

Peter MCS. Understanding the adaptive response in vertebrates: The phenomenon of ease and ease response during post-stress acclimation. Gen Comp Endocrinol. 2013; 181:59-64. https://doi.org/10.1016/j.ygcen.2012.09.016

Peter MCS, Anand SB, Peter VS. Stress tolerance in fenvalerate-exposed air-breathing perch: thyroidal and ionoregulatory responses. Proc Indian Environ Congr. 2004; pp. 294-98.

Barton BA. Stress in fishes: A diversity of responses with particular reference to changes in circulating corticosteroids. Integrt Comp Biol. 2002; 42:517-25. https://doi. org/10.1093/icb/42.3.517

Leji J, Babitha GS, Rejitha V, Ignatius J, Peter VS, Oommen OV. Thyroidal and osmoregulatory responses in tilapia (Oreochromis mossambicus) to the effluents of coconut husk retting. J Endocrinol Reprod. 2007; 11:24-31.

Vijayan MM, Pereira C, Forsyth RB, Kennedy CK, Iwama, GK. Handling stress does not affect the expression of hepatic heat shock protein 70 and conjugation enzymes in rainbow trout treated with α- napthoflavone. Life Sci. 1997; 61:117-27. https://doi.org/10.1016/S0024-3205(97)00366-4

George N, Peter MCS, Peter VS. Physiologic implications of inter-hormonal interference in fish: Lessons from the interaction of adrenaline with cortisol and thyroid hormones in climbing perch (Anabas testudineus Bloch). Gen Comp Endocrinol. 2013; 181:122-9. https://doi.org/10.1016/j. ygcen.2012.11.002

Peter MCS. Thyroid hormones and intermediary metabolism in fish: influence of neem kernel extract, in: Singh RP, Chari MS, Raheja AK, Kraus W. (Eds.), Neem and Environment, Oxford and IBH Publishing Co., New Delhi, 1996; pp. 1189-98.

Rejitha V, Peter VS, Peter MCS. Short-term salinity acclimation demands thyroid hormone action in climbing perch (Anabas testudineus Bloch). J Endocrinol Reprod. 2009; 13:63-72.

Leatherland JF. Reflections on the thyroidology of fishes: from molecules to humankind. Guelph Ichtyol Rev. 1994; 2:1-64.

Oommen OV, Sunny F, Smita M, George JM, Sreejith P, Beyo RS, Divya L, Vijayasree AS, Manju M, Johnson C, Akbarsha MA. Endocrine regulation of metabolism, oxidative stress and reproduction: physiological implications of functional interactions. In: Maitra SK (ed) Hormone Biotechnology, Daya Publishing House, New Delhi. 2007; pp. 320-45.

Peter VS, Peter MCS. Influence of coconut husk retting effluent on metabolic, interrenal and thyroid functions in the air-breathing perch, Anabas testudineus Bloch. J Endocrinol Reprod. 2007; 11:8-14.

Oommen OV, Matty AJ. Metabolism in poikilotherms: Regulation by thyroid hormones. In: Maitra SK (ed), Frontiers in Environmental and Metabolic Endocrinology, The University of Burdwan, India. 1997; pp. 1-11.

Ip KY, Chew SF. Ammonia production, excretion, toxicity and defense in fish: a review. Front Physiol. 2010; 134:1-20. https://doi.org/10.3389/fphys.2010.00134

Graham JB. Air-breathing fishes: Evolution, diversity and adaptation. Academic Press. 1997; pp. 234-41.

McCormick SD. Endocrine control of osmoregulation in teleost fish. Am. Zool. 2001; 41:781-94. https://doi. org/10.1093/icb/41.4.781

Beyenbach KW, Wieczorek H. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. J Exp Biol. 2006; 209:577-89. https://doi. org/10.1242/jeb.02014


Refbacks

  • There are currently no refbacks.