JBM  Vol.7 No.11 , November 2019
Effects of 17β-Estradiol on Dopamine D2 Receptors in Thiamine-Deficient Female Rats: Consequences on Sucrose, Alcohol, Water Intakes and Body Weight
Abstract: Our previous studies showed that 17β-estradiol (E2) modulated dopamine D2 receptor in regulating body weight set-point. The aim of this study was to understand whether thiamine deficiency influenced the E2 modulation on dopamine D2 receptors, using bromocriptine mesylate (BR) and sulpiride (SUL) as selective central dopamine-D2 receptors agonist and antagonist respectively. We studied the E2-dopamine D2 receptors interferences in a 10-day thiamine-deficient female rats for which consumptions of water, sugar, alcohol and food were daily-recorded and their consequences on body weights assessed. Our results showed that the volume of water daily ingested doubled in thiamine-deficient female rats (OXT), while sugar and alcohol consumptions collapsed with decreased weight and food consumption. On the one hand, thiamine potentiated D2/BR activity (bromocriptine-activated D2 receptors) to induce sugar intake and inhibited the same D2/BR receptors to induce water intake. On the other hand, thiamine promoted D2/SUL receptors (sulpiride-inhibited D2 receptors) for enhanced alcohol intake, increased food consumption and weight gain. Taking together, thiamine modulated the actions of 17β-estradiol on both D2/BR and D2/SUL receptors activities.
Cite this paper: Silué, S. and Bâ, A. (2019) Effects of 17β-Estradiol on Dopamine D2 Receptors in Thiamine-Deficient Female Rats: Consequences on Sucrose, Alcohol, Water Intakes and Body Weight. Journal of Biosciences and Medicines, 7, 36-55. doi: 10.4236/jbm.2019.711004.

[1]   Jiménez-Jiménez, F.J., et al. (1999) Cerebrospinal Fluid Levels of Thiamine in Patients with Parkinson’s Disease. Neuroscience Letters, 271, 33-36.

[2]   Jordan, F. (2003) Current Mechanistic Understanding of Thiamin Diphosphate-Dependent Enzymatic Reactions. Natural Product Reports, 20, 184-201.

[3]   Butterworth, R.F. (2003) Thiamin Deficiency and Brain Disorders. Nutrition Research Reviews, 16, 277-284.

[4]   Bâ, A. (2008) Metabolic and Structural Role of Thiamine in Nervous Tissues. Cellular Molecular Neurobiology, 28, 923-931.

[5]   Bâ, A. (2013) Perinatal Thiamine Deficiency-Induced Spontaneous Abortion and Pup-Killing Responses in Rat Dams. Nutritional Neuroscience, 16, 69-77.

[6]   Hohmann, S. and Meacock, P.A. (1998) Thiamin Metabolism and Thiamin Diphosphate-Dependent Enzymes in the Yeast Saccharomyces cerevisiae: Genetic Regulation. Biochimica et Biophysica Acta, 1385, 201-219.

[7]   Spenser, I.D.W.R. (1997) Biosynthesis of Vitamin B1 (Thiamin): An Instance of Biochemical Diversity. Angewandte Chemie International Edition in English, 36, 1032- 1046.

[8]   Faou, P. and Tropschug, M.A. (2004) Neurospora crassa CyPBP37: A Cytosolic Stress Protein That Is Able to Replace Yeast Thi4p Function in the Synthesis of Vitamin B1. Journal of Molecular Biology, 344, 1147-1157.

[9]   Daubner, S.C., Le, T. and Wang, S. (2011) Tyrosine Hydroxylase and Regulation of Dopamine Synthesis. Archives of Biochemistry and Biophysics, 508, 1-12.

[10]   Nakagawasai, O., Yamadera, F., Iwasaki, K., Asao, T., Tan-No, K., Niijima, F., et al. (2007) Preventive Effect of Kami-Untanto on Performance in the Forced Swimming Test in Thiamine Deficient Mice: Relationship to Functions of Catecholaminergic Neurons. Behavioral Brain Research, 177, 315-321.

[11]   Sjöquist, B., Johnson, H.A., Neri, A. and Lindén, S. (1988) The Influence of Thiamine Deficiency and Ethanol on Rat Brain Catecholamines. Drug and Alcohol Dependence, 22, 187-193.

[12]   Trovero, F., Gobbi, M., Weil-Fuggaza, J., Besson, M.J., Brochet, D. and Pirot, S. (2000) Evidence for a Modulatory Effect of Sulbutiamine on Glutamatergic and Dopaminergic Cortical Transmissions in the Rat Brain. Neuroscience Letters, 292, 49-53.

[13]   Frédérich, M., Delvaux, D., Gigliobianco, T., Gangolf, M., Dive, G., Mazzucchelli, G., et al. (2009) Thiaminylated Adenine Nucleotides. Chemical Synthesis, Structural Characterization and Natural Occurrence. FEBS Journal, 276, 3256-3268.

[14]   Subramanian, S. and Adiga, P.R. (1999) Characterization and Hormonal Modulation of Immunoreactive Thiamin Carrier Protein Secreted by Adult Rat Leydig Cells in Vitro. Journal of Endocrinology, 162, 49-56.

[15]   Maharjan, S., Serova, L.I. and Sabban, E.L. (2010) Membrane-Initiated Estradiol Signaling Increases Tyrosine Hydroxylase Promoter Activity with ER Alpha in PC12 Cells. Journal of Neurochemistry, 112, 42-55.

[16]   Roepke, T.A., Qiu, J., Bosch, M.A., Rønnekleiv, O.K. and Kelly, M.J. (2009) Cross- Talk between Membrane-Initiated and Nuclear-Initiated Oestrogen Signalling in the Hypothalamus. Journal of Neuroendocrinology, 21, 263-270.

[17]   Maharjan, S., Serova, L. and Sabban, E.L. (2005) Transcriptional Regulation of Tyrosine Hydroxylase by Estrogen: Opposite Effects with Estrogen Receptors α and β and Interactions with Cyclic AMP. Journal of Neurochemistry, 93, 1502-1514.

[18]   Pasqualini, C., Weltzien, F.A., Vidal, B., Baloche, S., Rouget, C., Gilles, N., et al. (2009) Two Distinct Dopamine D2 Receptor Genes in the European Eel: Molecular Characterization Tissue-Specific Transcription Regulation by Sex Steroids. Endocrinology, 150, 1377-1392.

[19]   Wu, Z.B., Li, C.Z., Zong, X.Y., Su, Z.P., Zeng, Y.J. and Zhang, Y.Z. (2009) Correlation of Alternative Splicing of the D2 Dopamine Receptor mRNA and Estrogen Receptor mRNA in the Prolactinomas and Gonadotrope Tumors. Journal of Neuro-Oncology, 94, 135-139.

[20]   Bâ, A. Silué, S., Bamba, B., Bamba, L. and Gahié S.-V. (2018) Effects of Ovariectomy and 17β-Estradiol Replacement on Dopamine D2 Receptors in Female Rats: Consequences on Sucrose, Alcohol, Water Intakes and Body Weight. Journal of Behavioral and Brain Science, 8, 1-25.

[21]   Memo, M., Govoni, S., Carboni, E., Trabucchi, M. and Spano, P.F. (1983) Characterization of Stereospecifi Binding of 3H-(-) Sulpiride a Selective Antagonist at Dopamine-D2 Receptors in Rat CNS. Pharmacological Research Communications, 15, 191-199.

[22]   Defronzo, R.A. (2011) Bromocriptine: A Sympatholytic d2-Dopamine Agonist for the Treatment of Type 2 Diabetes. Diabetes Care, 34, 789-794.

[23]   Neil, J.J. and Robin, S. (1983) Comparative Effect of Estradiol Stereoisomer on Pimozide induced Catalepsi, Locomotor Activity and Body-Weight in the Rat. Pharmacology Biochemistry and Behavior, 19, 801-805.

[24]   Fuller, R.W., Clemens, J.A. and Hynes, M.D. (1982) Degree of Selectivity of Pergolide as an Agonist at Presynaptic Dopamine Receptors: Implicattions for prevention or Treatment of Tardive Dyskinesia. Journal of Clinical Psychopharmacology, 6, 371-375.

[25]   Baptista, T., Araujo de Baptista, E., Ying Kin, N.M., Beaulieu, S., Walker, D., Joober, R., et al. (2002) Comparative Effects of the Antipsychotics Sulpiride or Risperidone in Rats. I: Bodyweight, Food Intake, Body Composition, Hormones and Glucose Tolerance. Brain Research, 957, 144-151.

[26]   Yuan, C., Gao, J., Guo, J., Bai, L., Marshall, C., Cai, Z., et al. (2014) Dimethyl Sulfoxide Damages Mitochondrial Integrity and Membrane Potential in Cultured Astrocytes. PLoS ONE, 9, e107447.

[27]   Cook, C.C.H., Hallwood, P.M. and Thomson, A.D. (1998) B Vitamin Deficiency and Neuropsychiatric Syndromes in Alcohol Misuse. Alcohol and Alcoholism, 35, 2-7.

[28]   Wayne, W.D. (1987) Biostatistics a Foundation for Analysis in the Health Sciences. 4th Edition, John Wiley & Sons, New York.

[29]   Smith, D.K., Ovesen, L., Chu, R., Sackel, S. and Howard, L. (1983) Hypothermia in a Patient with Anorexia Nervosa. Metabolism, 32, 1151-1154.

[30]   Molina, P.E., et al. (1994) Thiamin Deficiency Impairs Endotoxin-Induced Increases in Hepatic Glucose Output. American Journal of Clinical Nutrition, 59, 1045-1049.

[31]   Nadal, A., et al. (2009) The Pancreatic Beta-Cell as a Target of Estrogens and Xenoestrogens: Implications for Blood Glucose Homeostasis and Diabetes. Molecular and Cellular Endocrinology, 304, 63-68.

[32]   Rathanaswami, P., Pourany, A. and Sundaresan, R. (1991) Effects of Thiamine Deficiency on the Secretion of Insulin and the Metabolism of Glucose in Isolated Rat Pancreatic Islets. Biochemistry International, 25, 577-583.

[33]   Singh, M. (1982) Effect of Thiamin Deficiency on Pancreatic Acinar Cell Function. American Journal of Clinical Nutrition, 36, 500-504.

[34]   Srinivasan, P., Subramanian, V.S. and Said, H.M. (2014) Mechanisms Involved in the Inhibitory Effect of Chronic Alcohol Exposure on Pancreatic Acinar Thiamin Uptake. American Journal of Physiology Gastrointestinal and Liver Physiology, 306, G631-G639.

[35]   Pomero, F., Molinar, M.A., La Selva, M., Allione, A., Molinatti, G.M. and Porta, M. (2001) Benfotiamine Is Similar to Thiamine in Correcting Endothelial Cell Defects Induced by High Glucose. Acta Diabetologica, 38, 135-138.

[36]   Wu, S. and Ren, J. (2006) Benfotiamine Alleviates Diabetes-Induced Cerebral Oxidative Damage Independent of Advanced Glycation End-Product, Tissue Factor and TNF-Alpha. Neuroscience Letters, 394, 158-162.

[37]   Bâ, A. (2012) Effects of Thiamine Deficiency on Food Intake and Body Weight Increment in Adult Female and Growing Rats. Behavioural Pharmacology, 23, 575- 581.

[38]   Bâ, A. (2017) Alcohol and Thiamine Deficiency Trigger Differential Mitochondrial Transition Pore Opening Mediating Cellular Death. Apoptosis, 22, 741-752.

[39]   Burdakov, D., Luckman, S.M. and Verkhratsky, A. (2005) Glucose-Sensing Neurons of the Hypothalamus. Philosophical Transaction of Royal Society London Biological Sciences, 360, 2227-2235.

[40]   Carruthers, A., DeZutter, J., Ganguly, A. and Devaskar, S.U. (2009) Will the Original Glucose Transporter Isoform Please Stand up! American Journal of Physiology. Endocrinology and Metabolism, 297, E836-E848.

[41]   Simpson, I.A., Appel, N.M., Hokari, M., Oki, J., Holman, G.D., Maher, F., et al. (1999) Blood-Brain Barrier Glucose Transporter: Effects of Hypo- and Hyper-gly- cemia Revisited. Journal of Neurochemistry, 72, 238-247.

[42]   Holmquist, L., Stuchbury, G., Berbaum, K., Muscat, S., Young, S., Hager, K., et al. (2007) Lipoic acid as a Novel Treatment for Alzheimer’s Disease and Related Dementias. Pharmacology & Therapeutics, 113, 154-164.

[43]   Brinton, R.D., Chen, S., Montoya, M., Hsieh, D., Minaya, J., Kim, J., et al. (2000) The Women’s Health Initiative Estrogen Replacement Therapy Is Neurotrophic and Neuroprotective. Neurobiology of Aging, 21, 475-496.

[44]   Irwin, R.W., Yao, J., To, J., Hamilton, R.T., Cadenas, E. and Brinton, R.D. (2012) Selective Oestrogen Receptor Modulators Differentially Potentiate Brain Mitochondrial Function. Journal of Neuroendocrinology, 24, 236-248.

[45]   Yao, J., Zhao, L., Mao, Z., Chen, S., Wong, K.C., To, J., et al. (2013) Potentiation of Brain Mitochondrial Function by S-Equol and R/S-Equol Estrogen Receptor Beta- Selective PhytoSERM Treatments. Brain Research, 1514, 128-141.

[46]   Tiano, J. and Mauvais-Jarvis, F. (2011) Importance of Oestrogen Receptors to Preserve Functional β-Cell Mass in Diabetes. Nature Reviews Endocrinology, 8, 342-351.

[47]   Ropero, A.B., Pang, Y., Alonso-Magdalena, P., Thomas, P. and Nadal A. (2012) Role of ERβ and GPR30 in the Endocrine Pancreas: A Matter of Estrogen Dose. Steroids, 77, 951-958.

[48]   Nadal, A., Alonso-Magdalena, P., Soriano, S., Ripoll, C., Fuentes, E., Quesada, I., et al. (2011) Role of Estrogen Receptors Alpha, Beta and GPER1/GPR30 in Pancreatic Beta-Cells. Frontiers in Bioscience, 16, 251-260.

[49]   Koricanac, G., Tepavcevic, S., Zakula, Z., Milosavljevic, T., Stojiljkovic, M. and Isenovic, E.R. (2011) Interference between Insulin and Estradiol Signaling Pathways in the Regulation of Cardiac eNOS and Na+/K+-ATPase. European Journal of Pharmacology, 655, 23-30.

[50]   Thorens, B. (2015) GLUT2, Glucose Sensing and Glucose Homeostasis. Diabetologia, 58, 221-232.

[51]   Bian C., Bai, B., Gao, Q., Li, S. and Zhao, Y. (2019) 17β-Estradiol Regulates Glucose Metabolism and Insulin Secretion in Rat Islets β Cells through GPER and Akt/ mTOR/GLUT2 Pathway. Frontiers in Endocrinology, 10, 531.

[52]   Kumar, R., Balhuizen, A., Amisten, S., Lundquist, I. and Salehi, A. (2011) Insulinotropic and Antidiabetic Effects of 17β-Estradiol and the GPR30 Agonist G-1 on Human Pancreatic Islets. Endocrinology, 152, 2568-2579.

[53]   Lopez Vicchi, F., Luque, G.M., Brie, B., Nogueira, J.P., Garcia Tornadu, I. and Becu-Villalobos, D. (2016) Dopaminergic Drugs in Type 2 Diabetes and Glucose Homeostasis. Pharmacological Research, 109, 74-80.

[54]   Brady, K.T. (1989) Weight Gain Associated with Psychotropic Drugs. South Medical Journal, 82, 611-617.

[55]   Huang, T.L. and Lu, C.H. (2007) Correlations between Weight Changes and Lipid Profile Changes in Schizophrenic Patients after Antipsychotics Therapy. Chang Gung Medical Journal, 30, 26-32.

[56]   Baptista, T., de Baptista, E.A., Lalonde, J., Plamondon, J., Kin, N.M., Beaulieu, S., et al. (2004) Comparative Effects of the Antipsychotics Sulpiride and Risperidone in Female Rats on Energy Balance, Body Composition, Fat Morphology and Macronutrient Selection. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 28, 1305-1311.

[57]   Mokdad, A.H., Serdula, M.K., Dietz, W.H., Bowman, B.A., Marks, J.S., Jeffrey, P., et al. (1999) The Spread of the Obesity Epidemic in the United States. The Journal of the American Medical Association, 282, 1519-1522.

[58]   Klenotich, S.J., Ho, E.V., McMurray, M.S., Server, C.H. and Dulawa, S.C. (2015) Dopamine D2/3 Receptor Antagonism Reduces Activity-Based Anorexia. Translational Psychiatry, 5, e613.

[59]   Parada, M.A., Hernandeza, L. and Hoebela, B.G. (1988) Sulpiride Injections in the Lateral Hypothalamus Induce Feeding and Drinking in Rats. Biochemistry and Behavior, 30, 917-923.

[60]   Fetissov, S.O., Meguid, M.M., Sato, T. and Zhang, L.-H. (2002) Expression of Dopaminergic Receptors in the Hypothalamus of Lean and Obese Zucker Rats and Food Intake. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 283, R905-R910.

[61]   Daskalopoulos, E.P., Lang, M.A., Marselos, M., Malliou, F. and Konstandi, M. (2012) D2-Dopaminergic Receptor-Linked Pathways: Critical Regulators of CYP3A, CYP2C, and CYP2D. Molecular Pharmacology, 82, 668-678.

[62]   Flatt, J.-P. (2001) Macronutrient Composition and Food Selection. Obesity Research, 9, 256S-262S.