Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-23T08:35:42.821Z Has data issue: false hasContentIssue false
  • English
  • Français

Leptin administration during lactation leads to different nutritional, biometric, hemodynamic, and cardiac outcomes in prepubertal and adult female Wistar rats

Published online by Cambridge University Press:  01 February 2021

Karyne Pollo de Souza ,
Samuel de Sousa Pedro ,
Nazareth Novaes Rocha ,
Emiliana Barbosa Marques  and
Christianne Bretas Vieira Scaramello Open the ORCID record for Christianne Bretas Vieira Scaramello [Opens in a new window]
Karyne Pollo de Souza
Affiliation:
Laboratory of Experimental Pharmacology, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Samuel de Sousa Pedro
Affiliation:
Laboratory of Experimental Pharmacology, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Nazareth Novaes Rocha
Affiliation:
Laboratory of Experimental Pharmacology, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Emiliana Barbosa Marques
Affiliation:
Laboratory of Experimental Pharmacology, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Christianne Bretas Vieira Scaramello*
Affiliation:
Laboratory of Experimental Pharmacology, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
*
Address for correspondence: Christianne Bretas Vieira Scaramello, Laboratory of Experimental Pharmacology/Department of Physiology and Pharmacology, room 204A, Fluminense Federal University, Professor Hernani Pires de Melo street, 101, São Domingos, Niterói, Rio de Janeiro, 24.210-130, Brazil. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Literature reports that insults, such as hormonal disturbances, during critical periods of development may modulate organism physiology and metabolism favoring cardiovascular diseases (CVDs) later in life. Studies show that leptin administration during lactation leads to cardiovascular dysfunction in young and adult male Wistar rats. However, there are sex differences regarding CVD. Thus, the present work aimed to investigate neonatal leptin administration’s consequences on different outcomes in female rats at prepubertal and adult age. Newborn Wistar female rats were divided into two groups, Leptin and Control, receiving daily subcutaneous injections of this adipokine (8 μg/100 g) or saline for the first 10 of 21 d of lactation. Nutritional, biometric, hemodynamic, and echocardiographic parameters, as well as maximal effort ergometer performance, were determined at postnatal days (PND) 30 and 150. Leptin group presented lower food intake (p = 0.0003) and higher feed efficiency (p = 0.0058) between PND 21 and 30. Differences concerning echocardiographic parameters revealed higher left ventricle internal diameter (LVID) in systole (p = 0.0051), as well as lower left ventricle ejection fraction (LVEF) (p = 0.0111) and fractional shortening (FS) (p = 0.0405) for this group at PND 30. Older rats treated with leptin during lactation presented only higher LVID in systole (p = 0.0270). Systolic blood pressure and maximum effort ergometer test performance was similar between groups at both ages. These data suggest that nutritional, biometric, and cardiac outcomes due to neonatal leptin administration in female rats are age-dependent.

Keywords

Lactationleptinadaptationphysiologicalcardiovascular diseasesfemale
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 6 , December 2021 , pp. 870 - 875
Copyright
© The Author(s), 2021. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barker, DJ. The origins of the developmental origins theory. J Intern Med. 2007; 261(5), 412–417.CrossRefGoogle ScholarPubMed
Reynolds, CM, Gray, C, Li, M, Segovia, SA, Vickers, MH. Early life nutrition and energy balance disorders in offspring in later life. Nutrients. 2015; 7(9), 8090–8111.CrossRefGoogle ScholarPubMed
Wells, JC. The thrifty phenotype: An adaptation in growth or metabolism? Am J Hum Biol. 2011; 23(1), 65–75.CrossRefGoogle ScholarPubMed
Langley-Evans, SC. Nutrition in early life and the programming of adult disease: a review. J Hum Nutr Diet. 2015; 28(1), 1–14.CrossRefGoogle ScholarPubMed
Crispi, F, Crovetto, F, Gratacos, E. Intrauterine growth restriction and later cardiovascular function. Early Hum Dev. 2018; 126, 23–27.CrossRefGoogle ScholarPubMed
Zebrowski, DC, Jensen, CH, Becker, R, et al. Cardiac injury of the newborn mammalian heart accelerates cardiomyocyte terminal differentiation. Sci Rep. 2017; 7(1), 8362.CrossRefGoogle ScholarPubMed
Senyo, SE, Lee, RT, Kühn, B. Cardiac regeneration based on mechanisms of cardiomyocyte proliferation and differentiation. Stem Cell Res. 2014; 13(3 Pt B), 532–541.CrossRefGoogle ScholarPubMed
Schuster, S, Hechler, C, Gebauer, C, Kiess, W, Kratzsch, J. Leptin in maternal serum and breast milk: association with infants’ body weight gain in a longitudinal study over 6 months of lactation. Pediatr Res. 2011; 70(6), 633–637.CrossRefGoogle Scholar
Fields, DA, George, B, Williams, M, et al. Associations between human breast milk hormones and adipocytokines and infant growth and body composition in the first 6 months of life. Pediatr Obes. 2017; 12 Suppl 1, 78–85.CrossRefGoogle Scholar
Casabiell, X, Pinheiro, V, Tome, MA, et al. Presence of leptin in colostrum and/or breast milk from lactating mothers: a potential role in the regulation of neonatal food intake. J Clin Endocr Metab. 1997; 82, 4270–4273.CrossRefGoogle ScholarPubMed
Teixeira, CV, Passos, MCF, Ramos, CF, Dutra, SCP, Moura, EG. Leptin serum concentration in rats whose mothers were submitted to malnutrition during lactation. J Nutr Biochem. 2002; 13, 493–498.CrossRefGoogle ScholarPubMed
Elias, CF, Purohit, D. Leptin signaling and circuits in puberty and fertility. Cell Mol Life Sci. 2013;70(5), 841–862.CrossRefGoogle ScholarPubMed
Trevenzoli, IH, Pinheiro, CR, Conceição, EP, et al. Programming of rat adrenal medulla by neonatal hyperleptinemia: adrenal morphology, catecholamine secretion, and leptin signaling pathway. Am J Physiol Endocrinol Metab. 2010; 298(5), E941–E949.CrossRefGoogle ScholarPubMed
Granado, M, Fuente-Martín, E, García-Cáceres, C, Argente, J, Chowen, JA. Leptin in early life: a key factor for the development of the adult metabolic profile. Obes Facts. 2012; 5(1), 138–150.CrossRefGoogle ScholarPubMed
Toste, FP, de Moura, EG, Lisboa, PC, et al. Neonatal leptin treatment programmes leptin hypothalamic resistance and intermediary metabolic parameters in adult rats. Br J Nutr. 2006; 95, 830–837.CrossRefGoogle ScholarPubMed
Marques, EB, Rocha, NN, Dos santos MC, Nascimento JH, Scaramello CBV. Cardiac programming in rats submitted to leptin treatment during lactation. Int J Cardiol. 2015; 181C, 141–143.CrossRefGoogle Scholar
Marques, EB, Pinto, LMO, Nascimento, JH, Scaramello, CBV. Spontaneous and Isoprenaline-Evoked response of isolated heart preparations from rats submitted to leptin treatment during lactation. Int J Cardiol. 2015; 195, 48–50.CrossRefGoogle ScholarPubMed
World Health Organization cardiovascular disease risk charts: revised models to estimate risk in 21 global regions. Lancet Glob Health. 2019.Google Scholar
Ventura-Clapier, R, Dworatzek, E, Seeland, U, et al. Sex in basic research: concepts in the cardiovascular field. Cardiovasc Res. 2017; 113, 711–724.CrossRefGoogle ScholarPubMed
Posa, A, Szabó, R, Kupai, K, et al. Cardioprotective effect of selective estrogen receptor modulator raloxifene are mediated by heme oxygenase in estrogen-deficient rat. Oxid Med Cell Longev. 2017; 2017, 2176749.CrossRefGoogle ScholarPubMed
Mehta, LS, Beckie, TM, DeVon, HA, et al. Acute myocardial infarction in women a scientific statement from the american heart association. Circulation. 2016; 133, 916–947.CrossRefGoogle ScholarPubMed
Souza, LL, de Moura, EG, Lisboa, PC. Does early weaning shape future endocrine and metabolic disorders? Lessons from animal models. J Dev Orig Health Dis. 2020; 3, 1–11.Google Scholar
Pietrobon, CB, Bertasso, IM, Silva, BS, et al. Body adiposity and endocrine profile of female wistar rats of distinct ages that were early weaned. Horm Metab Res. 2020; 52(1), 58–66.Google ScholarPubMed
Journal of the Brazilian Society of Laboratory Animal Science. Brazilian Society of Laboratory Animal Science (SBCAL). 2018; 6, 1.Google Scholar
Percie du Sert, N, Hurst, V, Ahluwalia, A, et al. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biol. 2020; 18(7), e3000410.CrossRefGoogle ScholarPubMed
Numan, M. Maternal behavior. In The physiology of reproduction (eds. Knobil, E, Neill, J), 1988; 1569–1645. Raven Press, Ltd, New York.Google Scholar
Li, N, Guenancia, C, Rigal, E, et al. Short-Term moderate diet restriction in adulthood can reverse oxidative, cardiovascular and metabolic alterations induced by postnatal overfeeding in mice. Sci Rep. 2016; 28(6), 308–317.Google Scholar
Bailoo, JD, Reichlin, TS, Würbel, H. Refinement of experimental design and conduct in laboratory animal research. ILAR Journal. 2014; 55(3), 383–391.CrossRefGoogle ScholarPubMed
Heijning, BJM, Oosting, A, Kegler, D, van der Beek, EM. An increased dietary supply of medium-chain fatty acids during early weaning in rodents prevents excessive fat accumulation in adulthood. Nutrients. 2017; 9, 631.CrossRefGoogle ScholarPubMed
Quinn, R. Comparing rat’s to human’s age: how old is my rat in people years? Nutrition. 2005; 21(6), 775–777.CrossRefGoogle ScholarPubMed
Araújo, GA, Farias, RS, Pedro, SS, et al. Overweight during lactation and its implications for biometric, nutritional and cardiovascular parameters of young and adult male and female rats. J Nutr Sci. 2020; 9(27), 1–9.CrossRefGoogle Scholar
Lang, RM, Bierig, M, Devereux, RB, et al. Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005; 18(12), 1440–1463.CrossRefGoogle ScholarPubMed
Wideman, CH, Murphy, HM. Constant light induces alterations in melatonin levels, food intake, feed efficiency, visceral adiposity, and circadian rhythms in rats. Nutr Neurosci. 2009; 12(5), 233–240.CrossRefGoogle ScholarPubMed
Hermsdorff, HHM, Vieira, MAQM, Monteiro, JBR. Leptin and its influence in the pathophysiology of eating disorders. Rev Nutr. 2006; 19(3), 369379.Google Scholar
Mendonça, LS, Moreira, JAR. The influence of hormones leptin and insulin in localized fat. Revista Científica da FHO|UNIARARAS. 2015, 3(2), 47–56.Google Scholar
Maior, AS. Hormonal regulation of food intake: a brief review. Revista de Medicina, Ribeirão Preto. 2012; 45(3), 303–309.Google Scholar
Litwak, SA, Wilson, JL, Chen, W, et al. Estradiol prevents fat accumulation and overcomes leptin resistance in female high-fat diet mice. Endocrinology. 2014, 155(11), 4447–4460.CrossRefGoogle ScholarPubMed
Acharya, KD, Gao, X, Bless, EP, Chen, J, Tetel, MJ. Estradiol and high fat diet associate with changes in gut microbiota in female ob/ob mice. Scientific RepoRtS. 2019; 9, 20192.CrossRefGoogle ScholarPubMed
Hong, J, Stubbins, RE, Smith, RR, Harvey, AE, Núñez, NP. Differential susceptibility to obesity between male, female and ovariectomized female mice. Nutr J. 2009; 8, 11.CrossRefGoogle ScholarPubMed
Clegg, DJ. Minireview: the year in review of estrogen regulation of metabolism. Mol Endocrinol. 2012; 26(12), 1957–1960.CrossRefGoogle ScholarPubMed
Sharma, G, Prossnitz, ER. G-Protein-Coupled Estrogen Receptor (GPER) and sex-specific metabolic homeostasis. Adv Exp Med Biol. 2017; 1043, 427–453.CrossRefGoogle ScholarPubMed
Matysková, R, Zelezná, B, Maixnerová, J, et al. Estradiol supplementation helps overcome central leptin resistance of ovariectomized mice on a high fat diet. Horm Metab Res. 2010; 42(3), 182–186.CrossRefGoogle ScholarPubMed
Leopoldo, AS, Lima-Leopoldo, AP, Nascimento, AF, et al. Classification of different degrees of adiposity in sedentary rats. Braz J of Med Biol Res. 2016; 49(4), e5028.CrossRefGoogle ScholarPubMed
Kleinert, M, Clemmensen, C, Hofmann, SM, et al. Animal models of obesity and diabetes mellitus. Nat Rev Endocrinol. 2018; 4, 140–162.CrossRefGoogle Scholar
Fouda, YB, Tom, ENL, Atsamo, AD, Bonabe, C, Dimo, T. Effects of stem bark aqueous extract of Fagara tessmannii Engl (Rutaceae) on cardiovascular risks related to monosodium glutamate-induced obesity in rat: In vivo and in vitro assessments. J of Ethnophar. 2020; 260(5), 112972.CrossRefGoogle ScholarPubMed
Trevenzoli, IH, Valle, MM, Machado, FB, et al. Neonatal hyperleptinaemia programmes adrenal medullary function in adult rats: effects on cardiovascular parameters. J Physiol. 2007; 580(2), 629–637.CrossRefGoogle ScholarPubMed
Simonds, SE, Pryor, JT, Ravussin, E, et al. Leptin mediates the increase in blood pressure associated with obesity. Cell. 2014; 159(6), 1404–1416.CrossRefGoogle ScholarPubMed
von Schnurbein, J, Manzoor, J, Brandt, S, et al. Leptin is not essential for obesity-associated hypertension. Obes Facts. 2019; 12(4), 460–475.CrossRefGoogle Scholar
Lakdawala, NK, Winterfield, JR, Funke, BH. Dilated cardiomyopathy. Circ Arrhythm Electrophysiol. 2013; 6(1), 228–237.CrossRefGoogle ScholarPubMed
Souza, NS, Dos-Santos, RC, Silveira, ALB, et al. Effects of autonomic balance and fluid and electrolyte changes on cardiac function in infarcted rats: a serial study of sexual dimorphism. Clin Exp Pharmacol Physiol. 2016; 43(4), 476–483.CrossRefGoogle ScholarPubMed
Yu, Y, Shun-Guang, W, Weiss, RM, Felder, RB. Sex differences in the central and peripheral manifestations of ischemia-induced heart failure in rats. Am J Physiol Heart Circ Physiol. 2018; 316(1), H70–H79.CrossRefGoogle ScholarPubMed
Kitzman, DW, Groban, L. Exercise intolerance. Heart Fail Clin. 2008; 4, 99–115.CrossRefGoogle ScholarPubMed
Rodrigues, B, Figueroa, DM, Mostarda, CT, et al. Maximal exercise test is a useful method for physical capacity and oxygen consumption determination in streptozotocin-diabetic rats. Cardiovasc Diabetol. 2007; 13, 6–38.Google Scholar
Wang, F, Keimig, T, He, Q, et al. Augmented healing process in female mice with acute myocardial infarction. Gend Med. 2007; 4, 230–247.CrossRefGoogle ScholarPubMed
Javeshghani, D, Schiffrin, EL, Sairam, MR, Touyz, RM. Potentiation of vascular oxidative stress and nitric oxide-mediated endothelial dysfunction by high-fat diet in a mouse model of estrogen deficiency and hyperandrogenemia. J Am Soc Hypertens. 2009; 3, 295–305.CrossRefGoogle Scholar
Dent, MR, Tappia, PS, Dhalla, NS. Gender differences in apoptotic signaling in heart failure due to volume overload. Apoptosis. 2010; 15, 499–510.CrossRefGoogle ScholarPubMed
Lagranha, CJ, Deschamps, A, Aponte, A, Steenbergen, C, Murphy, E. Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res. 2010; 106, 1681–1691.CrossRefGoogle ScholarPubMed
Patrizio, M, Marano, G. Gender differences in cardiac hypertrophic remodeling. Ann Ist Super Sanità. 2016, 52(2), 223–229.Google ScholarPubMed
Baka, T, Hodosy, J, Krajcirovicova, K, et al. 17β-Estradiol treatment reversed left ventricular dysfunction in castrated male rats: an echocardiographic study. Can J Physiol Pharmacol. 2018, 96(8), 850–854.CrossRefGoogle ScholarPubMed
Schuster, I, Mahmoodzadeh, S, Dworatzek, E, et al. Cardiomyocyte-Specific overexpression of oestrogen receptor beta improves survival and cardiac function after myocardial infarction in female and male mice. Clin Sci. 2016, 130, 365–376.CrossRefGoogle ScholarPubMed
Alencar, AK, da Silva, JS, Lin, M, et al. Effect of age, estrogen status, and late-life GPER activation on cardiac structure and function in the fischer344xbrown norway female rat. J Gerontol A Biol Sci Med Sci. 2017, 72, 152–162.CrossRefGoogle ScholarPubMed
Deschamps, AM, Murphy, E. Activation of a novel estrogen receptor, GPER, is cardioprotective in male and female rats. Am J Physiol Heart Circ Physiol. 2009; 297: H1806–H1813.CrossRefGoogle ScholarPubMed
Wang, J, Bingaman, S, Huxley, VH. Intrinsic sex-specific differences in microvascular endothelial cell phosphodiesterases. Am J Physiol Heart Circ Physiol. 2010; 298(4), H1146–H1154.CrossRefGoogle ScholarPubMed
Boutin-Ganache, I, Picard, S, Deschepper, CF. Distinct gene-sex interactions regulate adult rat cardiomyocyte width and length independently. Physiol Genomics. 2002; 12, 61–67.CrossRefGoogle ScholarPubMed
Decano, JL, Pasion, KA, Black, N, et al. Sex-Specific genetic determinants for arterial stiffness in Dahl salt-sensitive hypertensive rats. BMC Genet. 2016; 17, 19.CrossRefGoogle ScholarPubMed
Ngun, T, Ghahramani, N, Sánchez, FJ, Bocklandt, S, Vilain, E. The genetics of sex differences in brain and behavior. Front Neuroendocrinol. 2011; 32(2), 227–246.CrossRefGoogle ScholarPubMed