Deferred Feeding and Body Weight Responses to Short-Term Interruption of Fuel Acquisition: Impact of Estradiol

 

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Abstract

Short-term abstinence from food intake, planned or unplanned, is unavoidable in modern life, but negatively correlated with appetite control and obesity. This study investigated the role of estradiol in feeding and body weight (BW) reactions to short-span cessation of feeding. During acute 1–6-h re-feeding, 12-h food-deprived (FD), estradiol benzoate (EB)-implanted ovariectomized rats ate less food and gained less weight than FD animals implanted with oil (O). Full fed (FF)- and FD-EB consumed equal amounts of food over 24 h, but weight gain was greater in the latter; 24-h food intake and BW gain in FD-O exceeded FD-EB. Caudal fourth ventricular administration of the AMPK activator AICAR increased dorsal vagal complex AMPK activity in FD-EB and FD-O, but elicited dissimilar adjustments in hypothalamic metabolic neuropeptide transmitter expression, while respectively enhancing or reducing acute re-feeding in these animals and reversing FD-O weight gain. Drug-treated FD-EB and FD-O exhibited respective feeding and weight gain increases between 6–24 h. AICAR enhanced 24-h consumption in FD-EB vs. FF-EB, but cumulative intake and BW gain were greater in AICAR-treated FD-O vs. FD-EB. Results show that estradiol limits acute re-feeding after short-term feeding suspension, but augments acute re-feeding when energy depletion coincides with suspended feeding. This compound metabolic stress exerts steroid-dependent effects during later resumption of circadian-induced feeding, for example, increased consumption vs. weight gain in the presence vs. absence of estradiol. These studies provide novel evidence that estrogen mitigates acute and post-acute adverse effects of disrupted fuel acquisition on energy balance.

• References

• 1 Grimm ER, Steinle NI. Genetics of eating behavior: established and emerging concepts. Nutr Rev 2011; 69: 52-60
  CrossrefPubMedGoogle Scholar
• 2 Leidy HJ, Campbell WW. The effect of eating frequency on appetite control and food intake: brief synopsis of controlled feeding studies. J Nutr 2011; 141: 154-157
  CrossrefPubMedGoogle Scholar
• 3 Stote KS, Baer DJ, Spears K, Paul DR, Harris GK, Rumpler WV, Strycula P, Najjar SS, Ferrucci L. A controlled trial of reduced meal frequency without caloric restriction in healthy, normal-weight, middle-aged adults. Am J Clin Nutr 2007; 85: 981-988
  CrossrefPubMedGoogle Scholar
• 4 Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev 1992; 16: 235-272
  CrossrefPubMedGoogle Scholar
• 5 Ropero AB, Alonso-Magdalena P, Quesada I, Nadal A. The role of estrogen receptors in the control of energy and glucose homeostasis. Steroids 2008; 73: 874-879
  CrossrefPubMedGoogle Scholar
• 6 Foryst-Ludwig A, Kintscher U. Metabolic impact of estrogen signaling through ERalpha and ERbeta. J. Steroid Biochem Mol Biol 2010; 12: 74-81
  PubMedGoogle Scholar
• 7 Wade GN. Sex hormones, regulatory behaviors, and body weight. In: Advances in the Study of Behavior. Rosenblatt J, Hinde R, Shaw E, Beer C. (eds.) New York: Academic Press; 1976. Vol. 6. 201-279
  Google Scholar
• 8 Nance DM. The developmental and neural determinants of effects of estrogen on feeding behavior in the rat: a theoretical perspective. Neurosci Biobehav Rev 1983; 7: 189-211
  CrossrefPubMedGoogle Scholar
• 9 Butera PC. Estradiol and the control of food intake. Physiol Behav 2010; 99: 175-180
  CrossrefPubMedGoogle Scholar
• 10 Sieck GC, Nance DM, Gorski RA. Estrogen modification of feeding behavior in the female rat: influence of metabolic state. Physiol Behav 1978; 21: 893-897
  CrossrefPubMedGoogle Scholar
• 11 Berdanier CD. Effects of estrogen on the responses of male and female rats to starvation-refeeding. J Nutr 1981; 111: 1425-1429
  PubMedGoogle Scholar
• 12 Strubbe JH, Woods SC. The timing of meals. Psychol Rev 2004; 111: 128-141
  CrossrefPubMedGoogle Scholar
• 13 Thammacharoen S, Lutz TA, Geary N, Asarian L. Hindbrain administration of estradiol inhibits feeding and activates estrogen receptor-alpha-expressing cells in the nucleus tractus solitaries of ovariectomized rats. Endocrinology 2008; 149: 1609-1617
  CrossrefPubMedGoogle Scholar
• 14 Ibrahim BA, Tamrakar P, Gujar AD, Koshy Cherian A, Briski KP. Caudal fourth ventricular administration of the AMPK activator 5-aminoimiazole-4-carboxamide-riboside regulates glucose and counterregulatory hormone profiles, dorsal vagal complex metabolosensory neuron function, and hypothalamic Fos expression. J Neurosci Res 2013; 91: 1226-1238
  CrossrefPubMedGoogle Scholar
• 15 Hardie DG. Minireview: The AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 2003; 144: 5179-5183
  CrossrefPubMedGoogle Scholar
• 16 Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metabol 2005; 1: 15-25
  CrossrefPubMedGoogle Scholar
• 17 Briski KP, Marshall ES, Sylvester PW. Effects of estradiol on glucoprivic transactivation of catecholaminergic neurons in the female rat caudal brainstem. Neuroendocrinology 2001; 73: 369-377
  CrossrefPubMedGoogle Scholar
• 18 Butcher RL, Collins WE, Fugo NW. Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17β throughout the 4-day estrous cycle of the rat. Endocrinology 1974; 94: 1704-1708
  CrossrefPubMedGoogle Scholar
• 19 Briski KP, Nedungadi TP. Adaptation of feeding and counterregulatory hormone responses to intermediate insulin-induced hypoglycemia in the ovariectomized female rat: effects of estradiol. J Neuroendocrinol 2009; 21: 578-585
  CrossrefPubMedGoogle Scholar
• 20 Swanson LW. Brain Maps: Structure of the Rat Brain. Amsterdam: Elsevier; 1999
  Google Scholar
• 21 Cherian A, Briski KP. Quantitative RT PCR and immunoblot analyses reveal acclimated A2 noradrenergic neuron substrate fuel transporter, glucokinase, phosphoAMPK, and dopamine-beta-hydroxylase responses to hypoglycemia. J Neurosci Res 2011; 89: 1114-1124
  CrossrefPubMedGoogle Scholar
• 22 Cherian A, Briski KP. Estradiol regulates phosphoAMPK, glucokinase, sub-strate transporter, and dopamine-beta-hydroxylase adaptation to repeated insulin-induced hypoglycemia in female rat A2 noradrenergic neurons. J Neurosci Res 2012; 90: 1347-1358
  CrossrefPubMedGoogle Scholar
• 23 Hayes MR, Skibicka KP, Bence KK, Grill HJ. Dorsal hindbrain 5’-adenosine monophosphate-activated protein kinase as an intracellular mediator of energy balance. Endocrinology 2009; 150: 2175-2182
  CrossrefPubMedGoogle Scholar
• 24 Briski KP, Koshy Cherian A, Genabai NK, Vavaiya KV. In situ coexpression of glucose and monocarboxylate transporter mRNAs in metabolic-sensitive dorsal vagal complex catecholaminergic neurons: transcriptional reactivity to insulin-induced hypoglycemia (IIH) and caudal hindbrain glucose or lactate repletion during IIH. Neuroscience 2009; 164: 1152-1160
  CrossrefPubMedGoogle Scholar
• 25 Gujar AD, Ibrahim BA, Tamrakar P, Koshy Cherian A, Briski KP. Hindbrain lactostasis regulates hypothalamic AMPK activity and hypothalamic metabolic neurotransmitter mRNA and protein responses to hypoglycemia. Am J Physiol Regul Integ Comp Physiol 2014; 306: R457-R469
  CrossrefPubMedGoogle Scholar
• 26 Simerly RB, Chang C, Muramatsu M, Swanson LW. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 1990; 294: 76-95
  CrossrefPubMedGoogle Scholar
• 27 Haywood SA, Simonian SX, van der Beek EM, Bicknell RJ, Herbison AE. Fluctuating estrogen and progesterone receptor expression in brainstem norepinephrine neurons through the rat estrous cycle. Endocrinology 1999; 140: 3255-3263
  PubMedGoogle Scholar
• 28 Temel S, Lin W, Lakhlani S, Jennes L. Expression of estrogen receptor-alpha and cFos in norepinephrine and epinephrine neurons of young and middle-aged rats during the steroid-induced luteinizing hormone surge. Endocrinology 2002; 143: 3974-3983
  CrossrefPubMedGoogle Scholar
• 29 Nagatani S, Tsukamura H, Maeda K. Estrogen feedback needed at the paraventricular nucleus or A2 to suppress pulsatile luteinizing hormone release in fasting female rats. Endocrinology 1996; 135: 870-875
  PubMedGoogle Scholar
• 30 Briski KP, Nedungadi TP, Cherian A. Effects of hypoglycaemia on neuro-transmitter and receptor gene expression in arcuate neuropeptide Y/agouti-related peptide neurones. J. Neuroendocrinol 2010; 22: 599-607
  CrossrefPubMedGoogle Scholar
• 31 Xu L, Faulkner LD, Hill JW. Cross-talk between metabolism and reproduction: the role of POMC and SF-1 neurons. Front Endocrinol 2011; 2: 98
  PubMedGoogle Scholar
• 32 Della Torre S, Benedusi V, Fontana V, Maggi A. Energy metabolism and fertility – a balance preserved for female health. Nat Rev Endocrinol 2014; 10: 13-23
  PubMedGoogle Scholar