Journal of Endocrinology and Reproduction

Open Access Open Access  Restricted Access Subscription Access
Open Access Open Access Open Access  Restricted Access Restricted Access Subscription Access

Rapid In Situ Action of Estradiol 17β on Ion Transporter Function in Brain Segments of Female Mozambique Tilapia (Oreochromis mossambicus Peters)


Affiliations
1 Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India
2 Inter-University Centre for Evolutionary and Integrative Biology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India
     

   Subscribe/Renew Journal


Being the principal estrogen, estradiol 17β (E2) is essential for normal ovarian function in the vertebrates including fishes. Besides its primary role in reproduction, E2 is also known for its role in many other physiological processes including water and mineral balance. However, it is uncertain, how E2 regulates ion-specific ATPases that drive Na+, K+, H+, Ca2+ and Mg2+ transport in fish brain. We, therefore, examined the short-term in situ action of E2 on ion transporter function in the brain segments of freshwater female Mozambique tilapia Oreochromis mossambicus. Tilapia were perfused with increasing doses of E2 (10-9, 10-8 and 10-7 M) for 20 min and sampled for determining Na+/K+-ATPase, H+-ATPase, Ca2+-ATPase, and Mg2+-ATPase activities in the prosencephalon (PC), mesencephalon (MC) and metencephalon (MeC) segments of brain. Dose-dependent increase in Na+/K+- and Ca2+-dependent transporter activities after E2 perfusion were found in PC. In MC, E2 treatment, however, produced significant increase in Mg2+, Ca2+ and H+ transport activities in mitochondria but decreased Na+/K+- and νH+ transporter activities. On the contrary, in MeC, E2 administration while producing increase in Na+/K+-, mitochondrial- and νH+-transport, lowered cytosolic and mitochondrial Ca2+ transport. Taken together, the data indicate that E2 has rapid and direct action on ion transporter function that corresponds to the differential activation/inactivation of neuronal clusters in the brain segments of female freshwater tilapia.

Keywords

Na+/K+-ATPase, Estradiol 17β, Fish, Ion Transporter, Ionoregulation, Tilapia brain.
Subscription Login to verify subscription
User
Notifications
Font Size


  • Pottinger TG, Carrick TR, Hughes SE, Balm PHM. Testosterone, 11-ketotestosterone, and estradiol-17β modify baseline and stress induced interrenal and corticotropic activity in trout. Gen Comp Endocrinol. 1996; 104: 284–295.

  • Cuesta A, Vargas-Chacoff, Garcia-Lopez A, Arjona FJ, Martinez-Rodriguez G, Meseguer J, Mancera JM, Esteban MA. Effect of sex-steroid hormones, testosterone and estradiol, on humoral immune parameters of gilthead seabream. Fish Shellfish Immunol. 2007; 23: 693–700.

  • Flouriot G, Pakdel F, Ducouret B, Ledrean Y, Valotaire, Y. Differential regulation of two genes implicated in fish reproduction: vitellogenin and estrogen receptor genes. Mol Reprod Dev. 1997; 48: 317–323.

  • Hu J, Zhang Z, Shen WJ, Azhar S. Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones. Nutr Metab. 2010; 7: 47.

  • Thomas P. Rapid steroid hormone actions initiated at the cell surface and the receptors that mediate them with an emphasis on recent progress in fish models. Gen Comp Endocrinol. 2012; 175: 367–383.

  • Evans PD, Bayliss A, Reale V. GPCR-mediated rapid, non-genomic actions of steroids: Comparisons between DmDopEcR and GPER1 (GPR30). Gen Comp Endocrinol. 2014; 195: 157–163.

  • Couse JF, Korach KS. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev. 1999; 20: 358– 417.

  • Saint-Criq V, Rapetti-Mauss R, Yusef YR, Harvey BJ. Estrogen regulation of epithelial ion transport: Implications in health and disease. Steroids. 2012; 77: 918–923.

  • Sunny F, Oommen OV. Effects of steroid hormones on total brain Na+/K+- ATPase activity in Oreochromis mossambicus. Indian J Exp Biol. 2004; 42: 283–287.

  • Fuzzen LM, Nicholas JB, Glen Van Der K. Differential effects of 17β-estradiol and 11-ketotestosterone on the endocrine stress response in zebrafish (Danio rerio). Gen Comp Endocrinol. 2011; 170: 365–373.

  • Bone Q, Moore RH. Nervous System. In: Elizabeth Owen. (Ed) Biology of Fishes, 3rd edn. Taylor and Francis group, UK. 2008; p. 346–383.

  • Peter MCS, Simi S. Hypoxia stress modifies Na+/K+-ATPase, H+/K+-ATPase, Na+/NH4+-ATPase, and nkaα1 isoform expression in the brain of immune-challenged air-breathing fish. J Exp Neurosci. 2017; 11: 1–18.

  • McIlwain H, Bachelard H.S. Biochemistry and the Central Nervous System. 4th Edn. Chruchill, London. 1971.

  • Bachelard HS. Outline Studies in Biology: Brain Biochemistry. Chapman and Hall, London.1974; p. 1-8.

  • Deshmukh PR, Bul SV, Gadhikar YA. Nuclear organization and distribution in the brain regions of the snake headed fish, Channa marulius. Ann Neurosci. 2011; 18: 92–99.

  • Lagler KF, Bardach JE, Miller RR. Ichthyology, John Wiley and Son, USA.1962; 545pp.

  • Nieuwenhuys R. An overview of the organization of the brain of actinopterygian fishes. Amer Zool. 1982; 22: 287– 310.

  • Kuhlenbeck H. The Central Nervous System of Vertebrates, Vol. 4. Spinal Cord and Deuterencephalon. Basel, Karger, 1975; 4: 388-623.

  • Samuel A, Peter VS, Peter MCS. Effect of L-tryptophan feeding on brain mitochondrial ion transport in netconfined climbing perch (Anabas testudineus Bloch). J Endocrinol Reprod. 2014; 18: 17.

  • Forlano PM, Schlinger BA, Bass AH. Brain aromatase: new lessons from non-mammalian model systems. Front Neuroendocrinol. 2006; 27: 247–274.

  • Do Rego JL, Seong JY, Burel D, Leprince J, Luu-The V, Tsutsui K, Tonon MC, Pelletier G, Vaudry H. Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front Neuroendocrinol. 2009; 30: 259–301.

  • DonCarlos LL, Azcoitia I, Garcia-Segura LM. Neuroprotective actions of selective estrogen receptor modulators. Psychoneuroendocrinology. 2009; 34S: S113-S122.

  • Garcia-Segura LM, Melcangi RC. Steroids and glial cell function. Glia. 2006; 54: 485–498.

  • Woolley CS. Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol. 2007; 47: 657–680.

  • Spencer JL, Waters EM, Romeo RD, Wood GE, Milner TA, McEwen BS. Uncovering the mechanisms of estrogen effects on hippocampal function. Front Neuroendocrinol. 2008; 29: 219–237.

  • Vegeto E, Benedusi V, Maggi A. Estrogen anti-inflammatory activity in brain: a therapeutic opportunity for menopause and neurodegenerative diseases. Front Neuroendocrinol. 2008; 29: 507–519.

  • Carbonell T, Rama R. Iron, oxidative stress and early neurological deterioration in ischemic stroke. Curr Med Chem. 2007; 14 : 857–874.

  • Venkataraman P, Krishnamoorthy G, Vengatesh G, Srinivasan N, Aruldhas MM, Arunakaran J. Protective role of melatonin on PCB (Aroclor 1254) induced oxidative stress and changes in acetylcholine esterase and membrane bound ATPases in cerebellum, cerebral cortex and hippocampus of adult rat brain. Int J Devl Neurosci. 2008; 26: 585–59.

  • Mahendravarma B, Surendrakumar RB. Enhancement of ATPases of fetal brain of mouse exposed to ultrasound. Biomedicine. 1996; 16: 27–33.

  • Erecinska M, Silver IA. Ions and energy in mammalian brain. Prog Neurobiol. 1994; 16: 37–71.

  • Carageorgiou H, Pantos C, Zarros A, Stolakis V, Mourouzis I, Cokkinos D, Tsakiris S. Changes in acetylcholinesterase, Na+/K+-ATPase, and Mg2+-ATPase activities in the frontal cortex and the hippocampus of hyper- and hypothyroid adult rats. Metab Clin Exp. 2007; 56: 1104–1110.

  • Sanui H, Rubin H. The role of magnesium in cell proliferation and transformation. In: Boynton, A.L., McKochan, W.L., Whitfield, J.P., (Eds.), Ions Cell Proliferation and Cancer, Academic Press, New York. 1982; pp. 517–537.

  • Simpkins JW, Wang J, Wang X, Perez E, Prokai L, Dykens JA. Mitochondria play a central role in estrogen-induced neuroprotection, Curr Drug Targets CNS Neurol Disord. 2005a; 4: 69–83.

  • Simpkins JW, Wen Y, Perez E, Yang S, Wang X. Role of nonfeminizing estrogens in brain protection from cerebral ischemia: an animal model of Alzheimer’s disease neuropathology. Ann N Y Acad Sci. 2005b; 1052: 233–242.

  • Simpkins JW, Yang SH, Sarkar SN, Pearce V. Estrogen actions on mitochondria-physiological and pathological implications. Mol Cell Endocrinol. 2008; 290: 51–59.

  • Brinton RD. The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci. 2008; 31: 529–537.

  • Yang SH, Liu R, Perez EJ, Wen Y, Stevens SM, Valencia T, Brun-Zinkernagel AM, Prokai L, Will Y, Dykens J, Koulen P, Simpkins JW. Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci U.S.A. 2004; 101: 4130– 4135.

  • Hwang PP, Lee TH, Weng CF, Fang MJ, Cho GY. Presence of Na+, K+-ATPase in mitochondria-rich cells in yolk-sac epithelium of larvae of the teleost, Oreochromis mossambicus. Physiol Biochem Zool. 1999; 72: 138–144.

  • Babitha GS, Peter MCS. Cortisol promotes and integrates the osmotic competence of the organs in North African catfish (Clarias gariepinus Burchell): Evidence from in vivo and in situ approaches. Gen Comp Endocrinol. 2010; 168: 14–21.

  • Lee CP, Sciamanna M, Peterson PL. Intact rat brain mitochondria from a single animal: preparation and properties. Methods Toxicol. 1993; 2: 41–50.

  • Veauvy CM, Wang Y, Walsh PJ, Perez-Pinson MA. Comparison of the effects of ammonia on brain mitochondrial function in rats and gulf toadfish. Am J Physiol Regul Integr Comp Physiol. 2002; 283: R598–R603.

  • Alexander JB, Ingram GA. A comparison of five methods commonly used to measure protein concentration of fish sera. J Fish Biol. 1980; 16: 115–122.

  • Peter MCS, Lock RAC, Wendelaar Bonga SE. Evidence for an osmoregulatory role of thyroid hormones in the freshwater Mozambique tilapia, Oreochromis mossambicus. Gen Comp Endocrinol. 2000; 120: 157–167.

  • Peter MCS, Leji J, Peter V S. 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: 225–231.

  • Ishihara Y, Takemoto T, Ishida A, Yamazaki T. Protective actions of 17β-estradiol and progesterone on oxidative neuronal injury induced by organometallic compounds. Oxid Med Cell Longev. 2015; 1–16

  • Lingrel JB, Orlowski J, Shull MM, Price EM. Molecular genetics of Na+/ K+-ATPase. Prog Nucleic Acid Res Mol Biol. 1990; 38: 37–89.

  • Albers RW, Siegel, GJ. Membrane transport, In: Brady ST, Siegel GJ, Albers RW, Price D, (Eds.). Basic Neurochemistry: Principles of Molecular, Cellular and Medical Neurobiology, 8th edn. Massachusetts, USA: Elsevier Academic Press. 2012; p. 41–62.

  • Beal MF. Aging, energy and oxidative stress in neurodegenerative diseases. Ann Neurol. 1995; 38: 357–366.

  • Lehotsky J, Kaplan P, Racay P, Matejovicova M, Drgova A, Mezesova V. Membrane ion transport systems during oxidative stress in rodent brain: Protective effect of stobadine and other antioxidants. Life Sci. 1999; 65: 1951–1958.

  • Jha R, Mahdi AA, Pandey S, Baquer NZ, Cowsik SM. Agerelated changes in membrane fluidity and fluorescence intensity by tachykinin neuropeptide NKB and Aβ (25 35) with 17β-estradiol in female rat brain. Am J Exp Clin Res.2014; 1: 25–30.

  • Man HY. The sodium pump: Novel functions in the brain. Biochem Anal Biochem. 2012;1: e116.

  • Wang X, Dykens JA, Perez E, Liu R, Yang S, Covey DF, Simpkins JW. Neuroprotective effects of 17β-estradiol and non-feminizing estrogens against H2 O2 toxicity in human neuroblastoma SK-N-SH cells. Mol Pharmacol. 2006; 70: 395–404.

  • Guerini D. The Ca2+ pumps and the Na+/Ca2+ exchangers. BioMetals. 1998; 11: 319–330.

  • Spitzer NC, Kingston PA, Manning TJ, Conklin MW. Outside and in: development of neuronal excitability. Curr Opin Neurobiol. 2002; 12: 315–323.

  • Zaidi A. Plasma membrane Ca2+-ATPases: Targets of oxidative stress in brain aging and neurodegeneration. World J Biol Chem. 2010; 1: 271–280.

  • Shutov L P, Kim MS, Houlihan P R, Medvedeva Y V, Usachev YM. Mitochondria and plasma membrane Ca2+-ATPase control presynaptic Ca2+clearance in capsaicin-sensitive rat sensory neurons. J Physiol. 2013; 591: 2443–2462.

  • de Sousa BN, Kendrick ZV, Roberts J, Baskin SI. Na+/ K+-ATPase in brain and spinal cord during aging. Adv Exp Med Biol. 1978; 97: 255-258.

  • Kumar P, Kale RK, Baquer NZ. Estradiol modulates membrane-linked ATPases, antioxidant enzymes, membrane fluidity, lipid peroxidation, and lipofuscin in aged rat liver. J Aging Res. 2011; 2011: 1–8.

  • Petrovic S, Milosevic M, Drakulic D, Grkovic I, Stanojlovic M, Mitrovic N, Horvat A 17β-Estradiol modulates mitochondrial Ca2+ flux in rat caudate nucleus and brain stem. Neuroscience. 2012; 220: 32–40.

  • Sanchez J C, Lopez-Zapata D F, Francis L, De Los Reyes L. Effects of estradiol and IGF-1 on the sodium calcium exchanger in rat cultured cortical neurons. Cell Mol Neurobiol. 2011; 31: 619–627.

  • Cipriano DJ, Wang Y, Bond S, Hinton A, Jefferies KC, Qi J, Forgac M. Structure and regulation of the vacuolar ATPases. Biochim Biophys Acta. 2008; 1777: 599–604.

  • Nelson N. Structure, molecular genetics, and evolution of vacuolar H+-ATPases. J Bioenerg Biomembr. 1989; 21: 553– 572.

  • Hammond C. Ionic gradients, membrane potential and ionic currents. Cell Mol Neurophysiol. 2015; 39–54.

  • Menzikov SA, Menzikova OV. Effects of orthovanadate and genistein on the plasma membrane Cl--ATPase sensitive to GABA-ergic ligands in the bream (Abramis brama L.) brain. Doklady Biol Sci. 2002; 385: 334–336.

  • Michaelis EK, Michaelis ML, Chang HH, Kitos TE. High affinity Ca2+-stimulated Mg2+-dependent ATPase in rat brain synaptosomes, synaptic membranes, and microsomes. J Biol Chem. 1983; 256: 6101–6108.

  • Cooper EC, Jan LY. Ion channel genes and human neurological disease, recent progress, prospects, and challenges. Proc Natl Acad Sci U.S.A. 1999; 96: 4759–4766.

  • Boyer DD, Chance B, Ernester L, Mitchell P, Racker E, Slater EC. Oxidative phosphorylation and photophosphorylation. Annu Rev Biochem. 1977; 46: 955–1026.


Abstract Views: 303

PDF Views: 0




  • Rapid In Situ Action of Estradiol 17β on Ion Transporter Function in Brain Segments of Female Mozambique Tilapia (Oreochromis mossambicus Peters)

Abstract Views: 303  |  PDF Views: 0

Authors

Dafina Wilfred
Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India
Valsa S. Peter
Inter-University Centre for Evolutionary and Integrative Biology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India
Subash Peter
Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India

Abstract


Being the principal estrogen, estradiol 17β (E2) is essential for normal ovarian function in the vertebrates including fishes. Besides its primary role in reproduction, E2 is also known for its role in many other physiological processes including water and mineral balance. However, it is uncertain, how E2 regulates ion-specific ATPases that drive Na+, K+, H+, Ca2+ and Mg2+ transport in fish brain. We, therefore, examined the short-term in situ action of E2 on ion transporter function in the brain segments of freshwater female Mozambique tilapia Oreochromis mossambicus. Tilapia were perfused with increasing doses of E2 (10-9, 10-8 and 10-7 M) for 20 min and sampled for determining Na+/K+-ATPase, H+-ATPase, Ca2+-ATPase, and Mg2+-ATPase activities in the prosencephalon (PC), mesencephalon (MC) and metencephalon (MeC) segments of brain. Dose-dependent increase in Na+/K+- and Ca2+-dependent transporter activities after E2 perfusion were found in PC. In MC, E2 treatment, however, produced significant increase in Mg2+, Ca2+ and H+ transport activities in mitochondria but decreased Na+/K+- and νH+ transporter activities. On the contrary, in MeC, E2 administration while producing increase in Na+/K+-, mitochondrial- and νH+-transport, lowered cytosolic and mitochondrial Ca2+ transport. Taken together, the data indicate that E2 has rapid and direct action on ion transporter function that corresponds to the differential activation/inactivation of neuronal clusters in the brain segments of female freshwater tilapia.

Keywords


Na+/K+-ATPase, Estradiol 17β, Fish, Ion Transporter, Ionoregulation, Tilapia brain.

References





DOI: https://doi.org/10.18311/jer%2F2017%2F23150