Maternal Prolactin Inhibition during Lactation Affects Physical Performance Evaluated by Acute Exhaustive Swimming Exercise in Adult Rat Offspring

G. Casimiro-Lopes; P. C. Lisboa; J. C. Koury; G. Boaventura; M.C. F. Passos; E. G. Moura

doi:10.1055/s-0031-1299711

Hormone and Metabolic Research, Table of Contents

Horm Metab Res 2012; 44(02): 123-129
DOI: 10.1055/s-0031-1299711

Animals

Maternal Prolactin Inhibition during Lactation Affects Physical Performance Evaluated by Acute Exhaustive Swimming Exercise in Adult Rat Offspring

Authors

G. Casimiro-Lopes

¹Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil
P. C. Lisboa

¹Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil
J. C. Koury

²Departamento de Nutrição Básica e Experimental, Instituto de Nutrição, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil
G. Boaventura

¹Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil
M.C. F. Passos

¹Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil
E. G. Moura

¹Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil

Abstract

Maternal prolactin inhibition at the end of lactation programs for metabolic syndrome and hypothyroidism in adult offspring, which could negatively affect exercise performance. We evaluated the effects of maternal hypoprolactinemia in late lactation on physical performance in adult progeny. Lactating Wistar rats were treated with bromocriptine (BRO, 1 mg per day) or saline on days 19, 20, and 21 of lactation and offspring were followed until 180 days old. Physical performance was recorded in untrained rats at 90 and 180 days by an acute exhaustive swimming test (exercise group-Ex). At day 90, BRO offspring showed higher visceral fat mass, higher plasma thiobarbituric acid reactive substances, lower total antioxidant capacity, higher liver glycogen, lower glycemia, and normal insulinemia. Although thyroid hormones (TH) levels were unchanged, mitochondrial glycerol phosphate dehydrogenase (mGPD) activity was lower in muscle and in brown adipose tissue (BAT). At this age, BRO-Ex offspring showed higher exercise capacity, lower blood lactate, higher serum T3, and higher muscle and BAT mGPD activities. At day 180, BRO offspring showed central obesity, hypothyroidism, insulin resistance, and lower EDL (extensor digitorum longus) muscle glycogen with unaltered plasma oxidative stress markers. This group showed no alteration of exercise capacity or blood lactate. After exercise, EDL and liver glycogen were lower, while T3 levels, BAT and muscle mGPD activities were normalized. Liver glycogen seem to be related with higher exercise capacity in younger BRO offspring, while the loss of this temporary advantage maybe related to the hypothyroidism and insulin resistance developed with age.

Key words

programming - exercise performance - oxidative stress - thyroid hormones - prolactin

Full Text

References

References
1 de Moura EG, Passos MCF. Neonatal programming of body weight regulation and energetic metabolism. Biosci Rep 2005; 25: 251-269
2 Moura EG, Santos RS, Lisboa PC, Alves SB, Bonomo IT, Fagundes AT, Oliveira E, Passos MC. Thyroid function and body weight programming by neonatal hyperthyroidism in rats – the role of leptin and deiodinase activities. Horm Metab Res 2008; 40: 1-7
3 Ravelli GP, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 1976; 295: 349-353
4 Passos MCF, Ramos CF, Moura EG. Short and long term effects of malnutrition in rats during lactation on the body weight of offspring. Nutr Res 2000; 20: 1603-1612
5 Lisboa PC, Passos MCF, Dutra SCP, Bonomo IT, Denolato ATA, Reis AM, Moura EG. Leptin and prolactin, but not corticosterone, modulate bodyweight and thyroid function in protein-malnourished lactating rats. Horm Metab Res 2006; 38: 1-5
6 Bonomo IT, Lisboa PC, Passos MC, Pazos-Moura CC, Reis AM, Moura EG. Prolactin inhibition in lactating rats changes leptin transfer through the milk. Horm Metab Res 2005; 37: 220-225
7 Bonomo IT, Lisboa PC, Pereira AR, Passos MC, de Moura EG. Prolactin inhibition in dams during lactation programs for overweight and leptin resistance in adult offspring. J Endocrinol 2007; 192: 339-344
8 Bonomo IT, Lisboa PC, Passos MCF, Alves SB, Moura EGM. Prolactin inhibition at the end of lactation programs for a central hypothyroidism in adult rat. J Endocrinol 2008; 198: 331-337
9 Moura EG, Bonomo IT, Nogueira-Neto JF, Oliveira E, Trevenzonli IH, Reis AM, Passos MCF, Lisboa PC. Maternal prolactin inhibition during lactation programs for metabolic syndrome in adult progeny. J Physiol 2009; 587: 4919-4929
10 Casimiro-Lopes G, Alves SB, Salerno VP, Passos MC, Lisboa PC, Moura EG. Maximum acute exercise tolerance in hyperthyroid and hypothyroid rats subjected to forced swimming. Horm Metab Res 2008; 40: 276-280
11 Zarzeczny R, Pilis W, Langfort J, Kaciuba-Uscilko H, Nazar K. Influence of thyroid hormones on exercise tolerance and lactate threshold in rats. J Physiol Pharmacol 1996; 47: 503-513
12 De Mello MAR. Effects of intrauterine and postnatal protein-calorie malnutrition on metabolic adaptations to exercise in young rats. Braz J Med Biol Res 1994; 27: 2461-2466
13 Oliveira E, Fagundes ATS, Alves SB, Pazos-Moura CC, Moura EG, Passos MCF, Lisboa PC. Chronic leptin treatment inhibits liver mitochondrial α-glycerol-3-phosphate dehydrogenase in euthyroid rats. Horm Metab Res 2007; 39: 867-870
14 Rasmussen UF, Krustrup P, Bangsbo J, Rasmussen HN. The effect of high-intensity exhaustive exercise studied in isolated mitochondria from human skeletal muscle. Pflügers Arch 2001; 443: 180-187
15 Venditti P, De Rosa R, DiMeo S. Effect of thyroid state on susceptibility to oxidants and swelling of mitochondria from rat tissues. Free Radic Biol Med 2003; 35: 485-494
16 Kutlu S, Canpolat S, Aydin M, Yasar A, Tuzcu M, Baydas G. Exogenous leptin increases lipid peroxidation in mouse brain. Tohoku J Exp Med 2005; 206: 233-236
17 Rastogi L, Godbole MM, Ray M, Rathore P, Pradhan S, Gupta SK, Pandey CM. Reduction in oxidative stress and cell death explains hypothyroidism induced neuroprotection subsequent to ischemia/reperfusion insult. Exp Neurol 2006; 200: 290-300
18 Monteiro R, Azevedo I. Chronic inflammation in obesity and the metabolic syndrome. Mediators Inflamm 2010; pii: 289645
19 Seiva FR, Berbert CM, Souza GA, Rocha KK, Ebaid GM, Burneiko RC, Novelli EL. Energy expenditure, lipid profile, oxidative stress, and cardiac energy metabolism after growth hormone treatment in obese young rats. Horm Metab Res 2010; 42: 496-501
20 Marques RG, Morales MM, Petroianu A. Brazilian law for scientific use of animals. Acta Cir Bras 2009; 24: 69-74
21 Lisboa PC, Pires L, de Oliveira E, Lima NS, Bonomo IT, Reis AM, Passos MC, Moura EG. Prolactin inhibition at mid-lactation influences adiposity and thyroid function in adult rats. Horm Metab Res 2010; 42: 562-569
22 Ahrén B, Scheurink AJW. Marked hyperleptinemia after high-fat diet associated with severe glucose intolerance in mice. Eur J Endocrinol 1998; 139: 461-467
23 Okhawa K, Vogt MT, Farber E. Unusually high mitochondrial alpha glycerophosphate dehydrogenase activity in rat brown adipose tissue. J Cell Biol 1969; 41: 441-449
24 Palmer JW, Tandler B, Höppel CL. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 1977; 252: 8731-8739
25 Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 1990; 186: 421-431
26 da Lima NS, de Moura EG, Passos MC, Nogueira Neto FJ, Reis AM, de Oliveira E, Lisboa PC. Early weaning causes undernutrition for a short period and programmes some metabolic syndrome components and leptin resistance in adult rat offspring. Br J Nutr 2011; 105: 1405-1413
27 Veskoukis AS, Nikolaidis MG, Kyparos A, Kokkinos D, Nepka C, Barbanis S, Kouretas D. Effects of xanthine oxidase inhibition on oxidative stress and swimming performance in rats. Appl Physiol Nutr Metab 2008; 33: 1140-1154
28 Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004; 114: 1752-1761
29 Reid M, Fadi B, Khawli A, Moody MR. Reactive oxygen in skeletal muscle. III. Contractility of unfatigued muscle. J Appl Physiol 1993; 75: 1081-1087
30 Gomez-Cabrera M, Borras C, Pallardo V, Sastre VF, Ji LL, Viña J. Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J Physiol 2005; 567: 113-120
31 Venditti P, Puca A, Di Meo S. Effect of thyroid state on rate and sites of H2O2 production in rat skeletal muscle mitochondria. Arch Biochem Biophys 2003; 411: 121-128
32 Tsintzas K, Williams C. Human muscle glycogen metabolism during exercise. Effect of carbohydrate supplementation. Sports Med 1998; 25: 7-23
33 Gleeson M, Waring JJ. Influence of diet on the storage, mobilization and utilization of energy reserves in trained and untrained rats. Comp Biochem Physiol A Comp Physiol 1986; 85: 411-415
34 Baldwin KM, Reitman JS, Terjung RL, Windler WW, Holloszy JO. Substrate depletion in different types of muscle and in liver during prolonged running. Am J Physiol 1973; 225: 1045-1050
35 Fortunato RS, Ignácio DL, Padron AS, Peçanha R, Marassi MP, Rosenthal D, Werneck-de-Castro JPS, Carvalho DP. The effect of acute exercise session on thyroid hormone economy in rats. J Endocrinol 2008; 198: 347-353
36 Lee Y, Lardy HA. Influence of thyroid hormones on l-alpha-glycerophosphate dehydrogenases and other dehydrogenases in various organs of the rat. J Biol Chem 1965; 240: 1427-1436
37 Dos Santos R, Alfadda A, Eto K, Kadowaki T, Silva JE. Evidence for a compensated thermogenic defect in transgenic mice lacking the mitochondrial glycerol-3-phosphate dehydrogenase gene. Endocrinology 2003; 144: 5469-5479
38 Sacktor R, Wormser-Shavit E, White JI. Diphosphopyridine nucleotide-linked cytoplasmic metabolites in rat leg muscle in situ during contraction and recovery. J Biol Chem 1965; 240: 2678-2681
39 Taleux N, Guigas B, Dubouchaud H, Moreno M, Weitzel JM, Goglia F, Favier R, Leverve XM. High expression of thyroid hormone receptors and mitochondrial glycerol-3-phosphate dehydrogenase in the liver is linked to enhanced fatty acid oxidation in Lou/C, a rat strain resistant to obesity. J Biol Chem 2009; 284: 4308-4316
40 Oh-ishi S, Kizaki T, Toshinai K, Haga S, Fukuda K, Nagata N, Ohno H. Swimming training improves brown-adipose-tissue activity in young and old mice. Mech Ageing Dev 1996; 89: 67-78
41 Pazos-Moura CC, Moura EG, Dorris ML, Rehnmark S, Melendez L, Silva JE, Taurog A. Effect of iodine deficiency and cold exposure on thyroxine 5′-deiodinase activity in various rat tissues. Am J Physiol 1991; 260: E175-E182