Body Adiposity and Endocrine Profile of Female Wistar Rats of
Distinct Ages that were Early Weaned
Carla Bruna Pietrobon‡
1
Laboratory of Endocrine Physiology, Biology Institute, State University
of Rio de Janeiro, RJ, Brazil
,
Iala Milene Bertasso‡
1
Laboratory of Endocrine Physiology, Biology Institute, State University
of Rio de Janeiro, RJ, Brazil
,
Beatrix S. Silva
1
Laboratory of Endocrine Physiology, Biology Institute, State University
of Rio de Janeiro, RJ, Brazil
,
Nayara Peixoto-Silva
1
Laboratory of Endocrine Physiology, Biology Institute, State University
of Rio de Janeiro, RJ, Brazil
,
Elaine Oliveira
1
Laboratory of Endocrine Physiology, Biology Institute, State University
of Rio de Janeiro, RJ, Brazil
,
Egberto Gaspar Moura
1
Laboratory of Endocrine Physiology, Biology Institute, State University
of Rio de Janeiro, RJ, Brazil
,
Patricia Cristina Lisboa
1
Laboratory of Endocrine Physiology, Biology Institute, State University
of Rio de Janeiro, RJ, Brazil
› InstitutsangabenFunding This research received financial support from National Council for Scientific and
Technological Development (CNPq), State of Rio de Janeiro Carlos Chagas Filho
Research Foundation (FAPERJ), and Coordination for the Enhancement of Higher
Education Personnel (CAPES).
Early weaning (EW) is a risk factor for metabolic syndrome. Male rats that were
precociously weaned present neonatal malnutrition and, in adulthood, developed
overweight, accumulation of body fat, dyslipidemia, changes in glycemic
homeostasis, hyperleptinemia, and increase of vitamin D. As metabolic profile of
early-weaned females is not known, we investigated the endocrine-metabolic
parameters in adolescence and adult female rats of 2 different EW models. Wistar
lactating rats and pups from both sexes were separated into 3 groups:
non-pharmacological EW (NPEW), dams were involved with a bandage interrupting
suckling in the last 3 days of lactation; pharmacological EW (PEW), dams were
bromocriptine-treated (0.5 mg/twice a day via intraperitoneal
injection) for 3 days before weaning; and control, dams whose pups ate milk
throughout lactation. At 21 days-old, NPEW and PEW females had lower body
weight. At 180 days-old, NPEW and PEW females showed higher feed efficiency,
weight gain, body fat percentage, and greater accumulation of gonadal and
retroperitoneal fat depots associated with adipocyte hypertrophy. NPEW females
also showed hyperphagia. Only NPEW females presented hyperleptinemia. Plasma
thyroid hormones and vitamin D were unchanged among EW females. Regarding sex
hormones, at 45 days-old, no change was found in EW females, while at 180
days-old, PEW females had hypoestrogenemia. EW increases the risk for obesity in
female rats in adulthood, as already demonstrated for males, although through
distinct mechanisms involving some hormones.
Key words
developmental plasticity -
fat mass -
leptin -
vitamin D -
thyroid hormones
References
1
Eidelman AI,
Schanler RJ,
Johnston M.
et al. Breastfeeding and the use of human milk. Pediatrics 2012; 129: 827-841
5
Pirilä S,
Saarinen-Pihkala UM,
Viljakainen H.
et al. Breastfeeding and determinants of adult body composition: A prospective study
from birth to young adulthood. Horm Res Paediatr 2012; 77: 281-290
6
Yin J,
Quinn S,
Dwyer T.
et al. Maternal diet, breastfeeding and adolescent body composition: A 16-year
prospective study. Eur J of Clin Nutr 2012; 66: 1329-1334
10
Horta BL,
Victora CG,
França GVA.
et al. Breastfeeding moderates FTO related adiposity: A birth cohort study with 30
years of follow-up. Sci Rep 2018; 8: 1-11
15
Villar J,
Ismail LC,
Urias ES.
et al. The satisfactory growth and development at 2 years of age of the
Intergrowth-21st Fetal Growth Standards cohort support its appropriateness for
constructing international standards. Am J Obstet Gynecol 2018; 218: 841-854
19
Bonomo IT,
Lisboa PC,
Pereira AR.
et al. Prolactin inhibition in dams during lactation programs for overweight and leptin
resistance in adult offspring. J Endocrinol 2007; 192: 339-344
21
Lima NS,
Moura EG,
Passos MCF.
et al. 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
22
Nobre JL,
Lisboa PC,
Lima NS.
et al. Calcium supplementation prevents obesity, hyperleptinaemia and hyperglycaemia in
adult rats programmed by early weaning. Br J Nutr 2012; 107: 979-988
24
Bonomo IT,
Lisboa PC,
Passos MC.
et al. Prolactin inhibition in lactating rats changes leptin transfer through the
milk. Horm Metab Res 2005; 37: 220-225
25
Lima NS,
Franco JG,
Peixoto-Silva N.
et al. Ilex paraguariensis (yerba mate) improves endocrine and metabolic disorders in
obese rats primed by early weaning. Eur J Nutr 2014; 53: 73-82
26
Peixoto-Silva N,
Conceição EP,
Carvalho JC.
et al. Does bromocriptine play a role in decreasing oxidative stress for early weaned
programmed obesity?. Life Sci 2014; 95: 14-21
27
Bonomo IT,
Lisboa PC,
Passos MC.
et al. Prolactin inhibition at the end of lactation programs for a central
hypothyroidism in adult rat. J Endocrinol 2008; 198: 331-337
28
Lima NS,
Moura EG,
Franco JG.
et al. Developmental plasticity of endocrine disorders in obesity model primed by early
weaning in dams. Horm Metab Res 2013; 45: 22-30
29
Pinheiro CR,
Oliveira E,
Trevenzoli IH.
et al. Developmental plasticity in adrenal function and leptin production primed by
nicotine exposure during lactation: Gender differences in rats. Horm Metab Res 2011; 43: 693-701
30
Lisboa PC,
Soares PN,
Peixoto TC.
et al. Effects of cigarette smoke exposure during suckling on food intake, fat mass,
hormones and biochemical profile of young and adult female rats. Endocrine 2017; 57: 60-71
32
Méndez-Giménez L,
Becerril S,
Moncada R.
et al. Sleeve gastrectomy reduces hepatic steatosis by improving the coordinated
regulation of aquaglyceroporins in adipose tissue and liver in obese rats. Obes Surg 2015; 25: 1723-1734
34
Kramer MS,
Matush L,
Vanilovich I.
et al. Effects of prolonged and exclusive breastfeeding on child height, weigth,
adiposity and blood pressure at age 6.5 y: Evidence from a large randomized
trial. Am J Clin Nutr 2008; 86: 1717-1721
36
Cable N,
Bartley M,
McMunn A.
et al. Gender differences in the effect of breastfeeding on adult psychological
well-being. Eur J Public Health 2012; 22: 653-658
37
Aune D,
Norat T,
Romundstad P.
et al. Breastfeeding and the maternal risk of type 2 diabetes: A systematic review and
dose-response meta-analysis of cohort studies. Nutr Metab Cardiovasc Dis 2014; 24: 107-115
38
Chowdhury R,
Sinha B,
Sankar MJ.
et al. Breastfeeding and maternal health outcomes: A systematic review and
meta-analysis. Acta Paediatr 2015; 104: 96-113
39
Horta BL,
Loret de Mola C,
Victora CG.
Long-term consequences of breastfeeding on cholesterol, obesity, systolic blood
pressure and type 2 diabetes: A systematic review and meta-analysis. Acta Paediatr 2015; 104: 30-37
40
Victora CG,
Horta BL,
Loret de Mola C.
et al. Association between breastfeeding and intelligence, educational attainment, and
income at 30 years of age: A prospective birth cohort study from Brazil. Lancet Glob Health 2015; 3: 199-205
41
Passos MC,
Vicente LL,
Lisboa PC.
et al. Absence of anorectic effect to acute peripheral leptin treatment in adult rats
whose mothers were malnourished during lactation. Horm Metab Res 2004; 36: 625-629
42
Vicente LL,
de Moura EG,
Lisboa PC.
et al. Malnutrition during lactation in rats is associated with higher expression of
leptin receptor in the pituitary of adult offspring. Nutrition 2004; 20: 924-928
43
Chandrika P,
Bhakhri BK,
Gathwala G.
et al. Risk factors for discontinuation of exclusive breastfeeding by one month of
postnatal age among high risk newborns: An institution based case control
study. J Clin Diagn Res 2015; 9: 1-3
44
Khandelwal P,
Jain V,
Gupta AK.
et al. Association of early postnatal growth trajectory with body composition in term
low birth weight infants. J Dev Orig Health Dis 2014; 5: 189-196
45
Nevin CL,
Formosa E,
Maki Y.
et al. Maternal nutrient restriction in guinea pigs as an animal model for studying
growth-restricted offspring with postnatal catch-up growth. Am J Physiol Regul Integr Comp Physiol 2018; 314: 647-654
46
Considine RV,
Considine EL,
Williams CJ.
et al. The hypothalamic leptin receptor in humans: Identification of incidental
sequence polymorphisms and absence of the db/db mouse and fa/fa
rat mutations. Diabetes 1996; 45: 992-994
47
Burguera B,
Couce ME,
Curran GL.
et al. Obesity is associated with a decreased leptin transport across the
blood–brain barrier in rats. Diabetes 2000; 49: 1219-1223
49
Farr OM,
Gavrieli A,
Mantzoros CS.
Leptin applications in 2015: What have we learned about leptin and obesity?. Curr Opin Endocrinol Diabetes Obes 2015; 22: 353-359
50
Younes-Rapozo V,
Moura EG,
Lima NS.
et al. Early weaning is associated with higher neuropeptide Y (NPY) and lower cocaine-
and amphetamine-regulated transcript (CART) expressions in the paraventricular
nucleus (PVN) in adulthood. Br J Nutr 2012; 108: 2286-2295
51
Conceição EP,
Trevenzoli IH,
Oliveira E.
et al. Higher white adipocyte area and lower leptin production in adult rats overfed
during lactation. Horm Metab Res 2011; 43: 513-516
52
Paz-Filho GJ,
Volaco A,
Suplicy HL.
et al. Decrease in leptin production by the adipose tissue in obesity associated with
severe metabolic syndrome. Arq Bras Endocrinol Metabol 2009; 53: 1088-1095
53
Chan JL,
Blüher S,
Yiannakouris N.
et al. Regulation of circulating soluble leptin receptor levels by gender, adiposity,
sex steroids, and leptin: Observational and interventional studies in
humans. Diabetes 2002; 51: 2105-2112
55
Brown LM,
Clegg DJ.
Central effects of estradiol in the regulation of food intake, body weight, and
adiposity. J Steroid Biochem Mol Biol 2010; 122: 65-73
56
Jenks MZ,
Fairfield HE,
Johnson EC.
et al. Sex steroid hormones regulate leptin transcript accumulation and protein
secretion in 3T3-L1 cells. Sci Rep 2017; 7: 8232
57
Pinos H,
Carrillo B,
Díaz F.
et al. Differential vulnerability to adverse nutritional conditions in male and female
rats: Modulatory role of estradiol during development. Front Neuroendocrinol 2018; 48: 13-22
58
Côte I,
Green SM,
Yarrow JF.
et al. Oestradiol and leptin have separate but additive anorexigenic effects and
differentially target fat mass in rats. J Nneuroendocrinol 2018; 30: 12646
59
Machinal F,
Dieudonne MN,
Leneveu MC.
et al. In vivo and in vitro ob gene expression and leptin secretion in rat adipocytes:
Evidence for a regional specific regulation by sex steroid hormones. Endocrinology 1999; 140: 1567-1574
60
Meli R,
Pacilio M,
Raso GM.
et al. Estrogen and raloxifene modulate leptin and its receptor in hypothalamus and
adipose tissue from ovariectomized rats. Endocrinology 2004; 145: 3115-3121
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