Horm Metab Res 2006; 38(5): 295-299
DOI: 10.1055/s-2006-925390
Original Basic
© Georg Thieme Verlag KG Stuttgart · New York

Leptin and Prolactin, but not Corticosterone, Modulate Body Weight and Thyroid Function in Protein-malnourished Lactating Rats

P.  C.  Lisboa1 , M.  C.  F.  Passos2 , S.  C.  P.  Dutra1 , I.  T.  Bonomo1 , A.  T.  A.  Denolato1 , A.  M.  Reis3 , E.  G.  Moura1
  • 1 Dept. Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brasil
  • 2 Dept. Nutrição Aplicada, Instituto de Nutrição, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brasil
  • 3 Dept. Fisiologia e Biofísica, ICB, Universidade Federal de Minas Gerais, MG, Brasil
Further Information

Publication History

Received 16 September 2005

Accepted after revision 20 December 2005

Publication Date:
23 May 2006 (online)

Abstract

To understand the role of hormonal changes in the lower food ingestion and body weight in protein-restricted lactating rats as well as the higher serum T3, higher deiodination, iodide and T3 milk transfer, we measured maternal serum prolactin, leptin, TSH and corticosterone, which are hormones that could influence those parameters. After birth, dams were separated into: control-fed with a 23 % protein diet (n = 12) and PR (protein-restricted)-fed with an 8 % protein diet (n = 12). At the 4th and 21st day of lactation, half of the animals in each group were sacrificed. PR dams presented hyperleptinemia (day 4: + 20 %; day 21: + 19 %; p < 0.05) and hypoprolactinemia (day 4: - 85 %; day 21: - 92 %; p < 0.05), which could help explain the lower food consumption and body weight in lactating PR rats since leptin is anorexigenic and prolactin is orexigenic. Also, this hyperleptinemia could contribute for the increase in serum T3 of PR dams, since leptin stimulates T3 production, especially acting on deiodinases. Serum corticosterone was not different between PR and C groups, and TSH was lower only at the end of lactation. Thus, we suggest that both leptin and prolactin could play an important role in the body weight and thyroid hormone changes observed in protein-malnourished lactating rats.

References

  • 1 LoPresti J S, Gray D, Nicoloff J T. Influence of fasting and refeeding on 3,3,5’-triiodothyronine metabolism in man.  Journal of Clinical Endocrinology and Metabolism. 1991;  72 130-134
  • 2 Harris A RC, Fang S L, Azizi F, Lipworth L, Vagenakis A G, Braverman L E. Effect of starvation on hypothalamic-pituitary-thyroid function in rat.  Metabolism. 1978;  27 1074-1083
  • 3 Moura E G, Ramos C F, Nascimento C CA, Rosenthal D, Breitenbach M MD. Thyroid function in fasting rats: variations in 131I uptake and transient decrease in peroxidase activity.  Brazilian Journal of Medical and Biological Research. 1997;  20 407-410
  • 4 Ramos C F, Teixeira C V, Passos M CF, Pazos-Moura C C, Lisboa P C, Curty F H, Moura E G. Low-protein diet changes thyroid function in lactating rats.  Proceedings of the Society for Experimental Biology and Medicine. 2000;  224 256-263
  • 5 Passos M CF, Ramos C F, Mouço T, Moura E G. Increase of T3 secreted through the milk in protein-restricted lactating rats.  Nutrition Research. 2001a;  21 917-924
  • 6 Passos M CF, Ramos C F, Dutra S CP, Moura E G. Transfer of iodine through the milk in protein-restricted lactating rats.  Journal of Nutritional Biochemistry. 2001b;  12 300-303
  • 7 Passos M CF, Ramos C F, Dutra S CP, Mouço T, Moura E G. Long-term effects of malnutrion during lactation on the thyroid function of offspring.  Horm Metab Res. 2002;  34 40-43
  • 8 Lisboa P C, Passos M CF, Dutra S CP, Santos R S, Bonomo I T, Cabanelas A P, Pazos-Moura C C, Moura E G. Increased 5’-iodothyronine deiodinase activity is a maternal adaptative mechanism in response to protein restriction during lactation.  Journal of Endocrinology. 2003a;  177 261-267
  • 9 Passos M CF, Ramos C F, Moura E G. Short and long term effects of malnutrition in rats during lactation on the body weight of offspring.  Nutr Res. 2000;  20 1603-1612
  • 10 Noel M B, Woodside B C. Effects of systemic and central prolactin injections on food intake, weight gain, and estrous cyclicity in female rats.  Physiol Behav. 1993;  54 151-154
  • 11 Heil S H. Sex-specific effects of prolactin on food by rats.  Horm Behav. 1999;  35 47-54
  • 12 Brichard S M, Delporte M L, Lambert M. Adipocytokines in anorexia nervosa: a review focusing on leptin and adiponectin.  Horm Metab Res. 2003;  35 337-342
  • 13 Popovic V, Duntas L H. Leptin, TRH and grelin: influence on energy homeostasis at rest and during exercise.  Horm Metab Res. 2005;  37 533-537
  • 14 Seoane L M, Carro E, Tovar S, Casanueva F F, Dieguez C. Regulation in vivo TSH secretion by leptin.  Regul Pept. 2000;  92 25-29
  • 15 Ortiga-Carvalho T M, Oliveira K J, Soares B A, Pazos-Moura C C. Leptin role in the regulation of thyrotropin secretion in fed state - in vivo and in vitro studies.  J Endocr. 2002;  174 121-125
  • 16 Kolaczinsky J W, Considine R V, Ohannesian J, Marco C, Opentanova I, Nyce M R, Myint M, Caro J F. Responses of leptin to short-term fasting and refeeding in humans: a link with ketogenesis but not ketones themselves.  Diabetes. 1996;  45 1511-1515
  • 17 Ahima R S, Prabakaran D, Mantzoros C, Qu D, Lowell B, Maratos-Flier E, Flier S J. Role of leptin in the neuroendocrine response to fasting.  Nature. 1996;  382 250-252
  • 18 Monaco M H, Donovan S N. Moderate food restriction reduces serum IGF-I and alters circulating IGF - binding protein profiles in lactating rats.  Endocrinol. 1997;  152 303-316
  • 19 Dewey K G. Maternal body composition, caloric restriction and exercise during lactation.  J Nutr. 1998;  128 379S-380S
  • 20 Chakravarty I, Sreedhar R, Ghosh K, Bulusi S. Circulating gonadotropin profile in severe cases of protein calorie malnutrition.  Fertil Steril. 1982;  37 650-654
  • 21 Bayne K. Revised Guide for the Care and Use of Laboratory Animals available.  Am Phys Soc Physiol. 1996;  39 208-211
  • 22 Reeves P G, Nielsen F H, Fahey G C. AIN-93 Purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76 rodent diet.  J Nutr. 1993;  123 1939-1951
  • 23 Fishbeck K L, Rasmussen K M. Effect of repeated cycles on maternal nutritional status, lactational performance and litter growth in ad libitum-fed and chronically food-restricted rats.  J Nutr. 1987;  117 1967-1975
  • 24 Mukherjea R, Castonguay T W, Douglass L W, Moser-Veillon P. Elevated leptin concentrations in pregnancy and lactation: possible role as a modulator of substrate utilization.  Life Sciences. 1999;  65 1183-1193
  • 25 Pickavance L, Tadayyon M, Williams G, Vernon R G. Lactation Suppresses Diurnal Rhythm of Serum Leptin. Biochem.  Biophys Res Commun. 1998;  248 196-199
  • 26 Amico J A, Thomas A, Crowley R S, Burneister L A. Concentrations of leptin in the serum of pregnant, lactating, and cycling rats and of leptin messenger ribonucleic acid in rats placental tissue.  Life Sci. 1998;  63 1387-1395
  • 27 Brogan R S, Mitchell S E, Trayhurn P, Smith M S. Supression of leptin during lactation: contribution of the suckling stimulus versus milk production.  Endocrinol. 1999;  140 2621-2627
  • 28 Denis R G, Williams G, Vernon R G. Regulation of serum leptin and its role in the hyperphagia of lactation in the rat.  J Endocrinol. 2003;  176 193-203
  • 29 Pelleymounter M A, Cullen M J, Baker M B, Hecht R, Winters D, Boone T. et al . Effects of the obese gene product on body weight regulation in ob/ob mice.  Science. 1995;  269 540-543
  • 30 Halaas J L, Boozer C, Blair-West J, Fidahusein N, Denton D A, Friedman J M. Physiological response to long-term peripheral and central leptin infusion in lean and obese mice.  Proc Natl Acad Sci USA. 1997;  94 8878-8883
  • 31 Schwartz M W, Peskind E, Raskind M, Boyko E J, Porte Jr D . Cerebrospinal fluid leptin levels: relationship to plasma levels and to adiposity in humans.  Nat Med. 1996;  2 589-593
  • 32 Smith-Kirwin S M, O’Connor D M, De Johnston J, De Lancey E D, Hassink S G, Funanage V L. Leptin expression in human mammary epithelial cells and breast milk.  J Clin Endocrinol Metab. 1998;  83 1810-1813
  • 33 Wang J, Liu R, Hawkins M, Barzilai N, Rossetti L. A nutrient-sensing pathway regulates leptin gene expression in muscle and fat.  Nature. 1998;  393 684-688
  • 34 Bado A, Levasseur S, Attoub S, Kermongant S, Laigneau J P, Bortoluzzi M N. et al . The stomach is a source of leptin.  Nature. 1998;  394 790-793
  • 35 Martin A, Berraondo B, Martinez J Á. Leptin: physiological actions.  J Physiol Biochem. 1999;  55 43-49
  • 36 Morash B, Li A, Murphy P R, Wilkinson M, Ur E. Leptin gene expression in the brain and pituitary gland.  Endocrinology. 1999;  1140 5995-5998
  • 37 Casabiell X, Piñeiro V, Tomé M A, Peinó R, Diéguez C, Casanueva F F. Presence of leptin in colostrum and/or breast milk from lactating mothers: a potencial role in the regulation of neonatal food intake.  J Clin Endocr Metab. 1997;  82 4270-4273
  • 38 Mantzoros C S, Moschos S J. Leptin in search of role in human physiology and pathophysiology.  Clin Endocrinol. 1998;  49 551-567
  • 39 Teixeira C V, Passos M CF, Ramos C F, Dutra S CP, Moura E G. Leptin serum concentration, food intake and body weight in rats whose mothers were exposed to malnutrition during lactation.  J Nutr Biochem. 2002;  13 493-498
  • 40 Legradi G, Emerson C H, Ahima R S, Flier J S, Lechan R M. Leptin prevents fasting-induced supression of prothyrotropin-releasing hormone messsenger ribonucleic acid in neurons of the hypothalamic paraventricular nucleus.  Endocrinology. 1997;  138 2569-2576
  • 41 Lisboa P C, Oliveira K J, Cabanelas A P, Ortiga-Carvalho T M, Pazos-Moura C C. Acute cold exposure, leptin and somatostatin analog (octreotide) modulate thyroid 5’-deiodinase.  American Journal of Physiology Endocrinology and Metabolism. 2003b;  284 E1172-E1176
  • 42 Nowak K M, Kaczmarek P, Mackowiak P, Ziolkowska A, Albertin G, Ginda W J, Trejter M, Nussdorfer G G, Malendowicz L K. Rat thyroid gland expresses the long form of leptin receptors, and leptin stimulates the function of the gland in euthyroid non-fasted animals.  Int J Mol Med. 2002;  9 31-34
  • 43 Heiman M L, Ahima R S, Craft L S, Schoner B, Stephens T W, Flier J S. Leptin inhibition of the hypothalamic-pituitary-adrenal axis in response to stress.  Endocrinology. 1997;  138 3859-3863
  • 44 Laud K, Gourdou I, Belair L, Keisler D H, Djiane J. Detection and regulation of leptin receptor in ovine mammary epithelial cells during pregnancy and lactation.  FEBS Letters. 1999;  463 194-198
  • 45 Vonderhaar B K, Greco A E. Lobulo-alveolar development of mouse mammary gland is regulated by thyroid hormones.  Endocrinol. 1979;  104 409-418
  • 46 Bhattacharjee M, Vonderhaar B K. Thyroid hormones enhance the synthesis and secretion of α-lactalbumin by mouse mammary tissue in vitro.  Endocrinol. 1984;  115 1070-1077
  • 47 Bonomo I T, Lisboa P C, Passos M CF, Pazos-Moura C C, Reis A M, Moura E G. Prolactin inhibition in lactating rats changes leptin transfer through the milk.  Horm Metab Res. 2005;  37 220-225

Dr. Egberto Gaspar de Moura

Departamento de Ciências Fisiológicas · 5° andar · Instituto de Biologia · Universidade do Estado do Rio de Janeiro

Av. 28 de setembro, 87 · Rio de Janeiro, RJ, 20551-030 · Brazil

Phone: +55 (21) 25 87 61 34

Fax: +55 (21) 25 87 61 29

Email: Egberto@Pesquisador.CNPQ.br

    >