Developmental Plasticity in Adrenal Function and Leptin Production Primed by Nicotine Exposure During Lactation: Gender Differences in Rats

C. R. Pinheiro; E. Oliveira; I. H. Trevenzoli; A. C. Manhães; A. P. Santos-Silva; V. Younes-Rapozo; S. Claudio-Neto; A. C. Santana; C.C. A. Nascimento-Saba; E. G. Moura; P. C. Lisboa

doi:10.1055/s-0031-1285909

Hormone and Metabolic Research, Table of Contents

Horm Metab Res 2011; 43(10): 693-701
DOI: 10.1055/s-0031-1285909

Original Basic

Georg Thieme Verlag KG Stuttgart · New York

Developmental Plasticity in Adrenal Function and Leptin Production Primed by Nicotine Exposure During Lactation: Gender Differences in Rats

C. R. Pinheiro

¹Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

E. Oliveira

¹Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

I. H. Trevenzoli

²Laboratory of Molecular Endocrinology, Federal University of Rio de Janeiro, RJ, Brazil

,

A. C. Manhães

³Laboratory of Neurophysiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

A. P. Santos-Silva

¹Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

V. Younes-Rapozo

¹Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

³Laboratory of Neurophysiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

S. Claudio-Neto

¹Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

³Laboratory of Neurophysiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

A. C. Santana

⁴Laboratory of Morphofunctional Analysis, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

C.C. A. Nascimento-Saba

⁴Laboratory of Morphofunctional Analysis, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

E. G. Moura

¹Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

,

P. C. Lisboa

¹Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, RJ, Brazil

› Author Affiliations

Abstract

Neonate male rats whose mothers were nicotine-treated during lactation have higher adiposity, hyperleptinemia, and adrenal dysfunction. At adulthood, they still present higher adiposity and hyperleptinemia, but there was no report about their adrenal function. Also, there was no report of this developmental plasticity on females. Here, we evaluated the adrenal function and leptin content in adipocytes and muscle of male and female adult offspring whose mothers were nicotine-treated during lactation. On the 2^nd postnatal day (PN2), dams were subcutaneously implanted with osmotic minipumps releasing nicotine (NIC-6 mg/kg/day) or saline for 14 days (12 litters/group and 2 rats/litter). Male and female offspring were killed on PN180. Significant data were p<0.05. Male NIC offspring presented higher adrenal catecholamine content (+ 89%) and TH expression (+ 38%), lower “in vitro” catecholamine release (− 19%), and higher adrenergic β3 receptor (ADRB3, + 59%) content in visceral adipose tissue (VAT). Serum corticosterone was higher (+ 77%) in male NIC group, coherent with the increase of both CRH and ACTH immunostaining in hypothalamus and pituitary, respectively. Leptin content was higher in VAT (+ 23%), which may justify the observed hyperleptinemia. Female NIC offspring presented lower ADRB3 content in VAT (− 39%) and lower leptin content in subcutaneous adipose tissue (SAT) (− 46%), but higher leptin content in soleus muscle (+ 22%), although leptinemia was normal. We evidenced a sex dimorphism in the model of maternal nicotine exposure during lactation. The adrenal function in adult offspring was primed only in male offspring while the female offspring displayed relevant alterations in leptin content on muscle and adipocytes.

Key words

catecholamine - corticosterone - adiposity - developmental plasticity

Full Text

References

References
1 Grun F, Blumberg B. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology 2006; 147: S50-S55
2 Tabb MM, Blumberg B. New modes of action for endocrine-disrupting chemicals. Mol Endocrinol 2006; 20: 475-482
3 Walsh RA. Effects of maternal smoking on adverse pregnancy outcomes: examination of the criteria of causation. Human Biol: Int Rec Res 1994; 6: 1059-1092
4 Oliveira E, Moura E, Santos-Silva A, Fagundes AT, Rios AS, Abreu-Villaça Y, Nogueira Neto JF, Passos MC, Lisboa PC. Short and long-term effects of maternal nicotine exposure during lactation on body adiposity, lipid profile and thyroid function of rat offspring. J Endocrinol 2009; 202: 397-405
5 Santos-Silva AP, Moura EG, Pinheiro CR, Rios AS, Abreu-Villaça Y, Passos MC, Oliveira E, Lisboa PC. Neonatal nicotine exposure alters leptin signaling in the hypothalamus-pituitary-thyroid axis in the late postnatal period and adulthood in rats. Life Sci 2010; 87: 187-195
6 Barker DJ. The developmental origins of adult disease. Eur J Epidemiol 2003; 18: 733-736
7 Moura EG, Passos MC. Neonatal programming of body weight regulation and energetic metabolism. Biosci Rep 2005; 25: 251-269
8 de Moura EG, Lisboa PC, Passos MC. Neonatal programming of neuroimmunomodulation role of adipocytokines and neuropeptides. Neuroimmunomodulation 2008; 15: 176-188
9 Gluckman PD, Hanson MA. Developmental plasticity and human disease: research directions. J Intern Med 2007; 261: 461-471
10 Grassi G, Seravalle G, Calhoun DA, Bolla GB, Giannattasio C, Mara M, Del Bo A, Mancia G. Mechanisms responsible for sympathetic activation by cigarette smoking in humans. Circulation 1994; 90: 248-253
11 Walker JF, Collins LC, Rowell PP, Goldsmith LJ, Moffatt RJ, Stamford BA. The effect of smoking on energy expenditure and plasma catecholamine and nicotine levels during light physical activity. Nicotine Tob Res 1999; 1: 365-370
12 Yeh J, Barbieri RL. Twenty four h urinary free cortisol in premenopausal cigarette smokers and nonsmokers. Fertil Steril 1989; 52: 1067-1069
13 Breese CR, Marks MJ, Logel J, Adams CE, Sullivan B, Collins AC, Leonard S. Effect of smoking history on [3H]nicotine binding in human postmortem brain. J Pharmacol Exp Ther 1997; 282: 7-13
14 Pauly JR, Grun EU, Collins AC. Tolerance to nicotine following chronic treatment by injections: a potential role for corticosterone. Psychopharmacology 1992; 108: 33-39
15 Sala F, Nistri A, Criado M. Nicotinic acetylcholine receptors of adrenal chromaffin cells. Acta Physiol (Oxf) 2008; 19: 203-212
16 Hiremagalur B, Nankova B, Nitahara J, Zeman R, Sabban EL. Nicotine increases expression of tyrosine hydroxylase gene. Involvement of protein kinase A-mediated pathway. J Biol Chem 1993; 268: 23704-23711
17 Slotkin TA, Seidler FJ. Acute and chronic effects of nicotine on synthesis and storage of catecholamines in the rat adrenal medulla. Life Sc 1975; 16: 1613-1622
18 Haycock JW. Phosphorylation of tyrosine hydroxylase in situ at serine 8, 19, 31, and 40. J Biol Chem 1990; 265: 11682-11691
19 Ahima RS, Saper CB, Flier JS, Elmquist JK. Leptin regulation of neuroendocrine systems. Front Neuroendocrinol 2000; 21: 263-307
20 Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature 1998; 395: 763-770
21 Sahu A. Leptin signaling in the hypothalamus: emphasis on energy homeostasis and leptin resistance. Front Neuroendocrinol 2003; 24: 225-253
22 Trevenzoli IH, Valle MMR, Machado FB, Garcia RMG, Passos MCF, Lisboa PC, Moura EG. Neonatal hyperleptinaemia programmes adrenal medullary function in adult rats: effects on cardiovascular parameters. J Physiol 2007; 580: 629-637
23 Trevenzoli IH, Rodrigues AL, Oliveira E, Thole AA, Carvalho L, Figueiredo MS, Toste FP, Neto JF, Passos MC, Lisboa PC, Moura EG. Leptin treatment during lactation programs leptin synthesis, intermediate metabolism, and liver microsteatosis in adult rats. Horm Metab Res 2010; 42: 483-490
24 Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL, Caro JF. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996; 334: 292-295
25 Takekoshi K, Motooka M, Isobe K, Nomura F, Manmoku T, Ishii K, Nakai T. Leptin directly stimulates catecholamine secretion and synthesis in cultured porcine adrenal medullary chromaffin cells. Biochem Biophys Res Commun 1999; 261: 426-431
26 Del Rio G. Adrenomedullary function and its regulation in obesity. Int J Obes Relat Metab Disord 2000; 24: S89-S91
27 Chen H, Vlahos R, Bozinovskil S, Jones J, Anderson GP, Morris MJ. Effect of short-term cigarette smoke exposure on body weight, appetite and brain neuropeptide Y in mice. Neuropsychopharmacology 2004; 30: 713-719
28 Oliveira E, Pinheiro CR, Santos-Silva AP, Trevenzoli IH, Abreu-Villaça Y, Nogueira Neto JF, Reis AM, Passos MC, Moura EG, Lisboa PC. Nicotine exposure affects mother’s and pup’s nutritional, biochemical, and hormonal profiles during lactation in rats. J Endocrinol 2010; 205: 159-170
29 Oliveira E, Moura E, Santos-Silva A, Pinheiro CR, Lima NS, Nogueira Neto JF, Nunes-Freitas AL, Abreu-Villaça Y, Passos MC, Lisboa PC. Neonatal nicotine exposure causes insulin and leptin resistance and inhibits hypothalamic leptin signaling in adult rat offspring. J Endocrinol 2010; 206: 55-63
30 Faraday MM, Blakeman KH, Grunberg NE. Strain and sex alter effects of stress and nicotine on feeding, body weight, and HPA axis hormones. Pharmacol Biochem Behav 2005; 80: 577-589
31 Marques RG, Morales MM, Petroianu A. Brazilian law for scientific use of animals. Acta Cir Bras 2009; 24: 69-74
32 Lichtensteiger W, Ribary U, Schlump FM, Odermatt B, Widmer HR. Prenatal adverse effects of nicotine on the developing brain. Progr Brain Res 1988; 73: 137-157
33 Toste FP, Moura EG, Lisboa PC, Fagundes AT, Oliveira E, Passos MCF. Neonatal leptin treatment programmes leptin hypothalamic resistance and intermediary metabolic parameters in adult rats. Br J Nutr 2006; 95: 830-837
34 Fagundes AT, Moura EG, Passos MC, Oliveira E, Toste FP, Bonomo IT, Trevenzoli IH, Garcia RM, Lisboa PC. Maternal low-protein diet during lactation programmes body composition and glucose homeostasis in the adult rat offspring. Br J Nutr 2007; 98: 922-928
35 Inoue M, Sakamoto Y, Fujishiro N, Imanaga I, Ozaki S, Prestwich GD, Warashina A. Homogeneous Ca²⁺ stores in rat adrenal chromaffin cells. Cell Calcium 2003; 33: 19-26
36 Fagundes AT, Moura EG, Passos MC, Santos-Silva AP, Oliveira ED, Trevenzoli IH, Casimiro Lopes G, Nogueira-Neto JF, Lisboa PC. Temporal evaluation of body composition, glucose homeostasis and lipid proﬁle of male rats programmed by maternal protein restriction during lactation. Horm Metab Res 2009; 41: 866-873
37 Trevenzoli IH, Pinheiro CR, Conceição EP, Oliveira E, Passos MC, Lisboa PC, Moura EG. Programming of rat adrenal medulla by neonatal hyperleptinemia: adrenal morphology, catecholamine secretion, and leptin signaling pathway. Am J Physiol Endocrinol Metab 2010; 298: E941-E949
38 Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York: Academic Press; 1998. 4th edition
39 Giglia R, Binns CW, Alfonso H. Maternal cigarette smoking and breastfeeding duration. Acta Paediatr 2006; 95: 1370-1374
40 McBride CM, Pirie PL. Postpartum smoking relapse. Addict Behav 1990; 15: 165-168
41 Hannöver W, Thyrian JR, Ebner A, Röske K, Grempler J, Kühl R, Hapke U, Fusch C, John U. Smoking during pregnancy and postpartum: smoking rates and intention to quit smoking or resume after pregnancy. J Womens Health (Larchmt) 2008; 17: 631-640
42 Narayanan U, Birru S, Vaglenova J, Breese CR. Nicotinic receptor expression following nicotine exposure via maternal milk. Neuroreport 2002; 13: 961-963
43 Utsunomiya K, Yanagihara N, Tachikawa E, Cheah TB, Kajiwara K, Toyohira Y, Ueno S, Izumi F. Stimulation of catecholamine synthesis in cultured bovine adrenal medullary cells by leptin. J Neurochem 2001; 76: 926-934
44 Takekoshi K, Ishii K, Kawakami Y, Isobe K, Nanmoku T, Nakai T. Ca(2+) mobilization, tyrosine hydroxylase activity, and signaling mechanisms in cultured porcine adrenal medullary chromaffin cells: effects of leptin. Endocrinology 2001; 142: 290-298
45 Clement K, Vaisse C, Manning BS, Basdevant A, Guy-Grand B, Ruiz J, Silver DK, Shuldiner RA, Froguel P, Strosberg DA. Genetic variation in the β3-adrenergic receptor and an increased capacity to gain weight in patients with morbid obesity. N Engl J Med 1995; 333: 352-354
46 Martins AC, Souza KL, Shio MT, Mathias PC, Lelkes PI, Garcia RM. Adrenal medullary function and expression of catecholamine-synthesizing enzymes in mice with hypothalamic obesity. Life Sci 2004; 74: 3211-3222
47 Marin P, Darin N, Amemiya T, Andersson B, Jern S, Björntorp P. Cortisol secretion in relation to body fat distribution in obese premenopausal women. Metabolism 1992; 41: 882-886
48 Rosmond R, Dallman MF, Björntorp P. Stress-related cortisol secretion in men: relationship with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab 1998; 83: 1853-1859
49 Livingstone DE, Jones GC, Smith K, Jamieson PM, Andrew R, Kenyon CJ, Walker BR. Understanding the role of glucocorticoids in obesity: tissue-specific alterations of corticosterone metabolism in obese Zucker rats. Endocrinology 2000; 141: 560-563
50 Couillard C, Mauriège P, Prudhomme D, Nadeau A, Tremblay A, Bouchard C, Després JP. Plasma leptin concentrations: gender differences and associations with metabolic risk factors for cardiovascular disease. Diabetologia 1997; 40: 1178-1184
51 Hassink SG, Sheslow DV, de Lancey E, Opentanova I, Considine RV, Caro JF. Serum leptin in children with obesity: relationship to gender and development. Pediatrics 1996; 98: 201-203
52 Mendelsohn ME, Karas RH. The protective effects of estrogen on the cardiovascular system. N Engl J Med 1999; 340: 1801-1811
53 Lovejoy JC. The menopause and obesity. Primary Care 2003; 30: 317-325