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Horm Metab Res 2017; 49(09): 707-715
DOI: 10.1055/s-0043-115394
Endocrine Research
© Georg Thieme Verlag KG Stuttgart · New York

Maternal High-Fat Diet During Pregnancy and Lactation has Opposite Effects on Gonadal Expression of Leptin and Leptin Receptor in Rat Dams and Their Offspring

Agnieszka Rak
1   Department of Physiology and Toxicology of Reproduction, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Krakow, Poland
,
Anna Hejmej
2   Department of Endocrinology, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Krakow, Poland
,
Monika Słupecka-Ziemilska
3   Department of Endocrinology, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Jabłonna, Poland
,
Jaroslaw Woliński
3   Department of Endocrinology, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Jabłonna, Poland
,
Elzbieta Fiedor
1   Department of Physiology and Toxicology of Reproduction, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Krakow, Poland
,
Barbara Bilinska
2   Department of Endocrinology, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Krakow, Poland
,
Ewa Ł. Gregoraszczuk
1   Department of Physiology and Toxicology of Reproduction, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Krakow, Poland
› Author Affiliations
Further Information

Publication History

received 26 February 2017

accepted 22 June 2017

Publication Date:
31 July 2017 (online)

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Correction: Maternal High-Fat Diet During Pregnancy and Lactation has Opposite Effects on Gonadal Expression of Leptin and Leptin Receptor in Rat Dams and Their OffspringHorm Metab Res 2017; 49(09): e2-e2
DOI: 10.1055/s-0037-1600932

Abstract

This study investigated the effect of a high-fat (HF) diet on protein expression of leptin and its receptor in the gonads of dams and their offspring. Female Wistar rats were fed a HF diet (30% fat) or a standard breeding (BD) diet (5% fat) during pregnancy and lactation. At 21 days of lactation, mothers and both sexes of prepubertal offspring were killed by decapitation. The protein expression of leptin and its receptor was assayed by Western blot and immunohistochemistry in gonadal, periovarian, and epididymal white adipose tissue (WAT). We demonstrated that leptin protein expression in ovary, and both leptin and ObRb expression in periovarian WAT was decreased in HF dams compared with BD animals. Immunohistochemistry showed lower leptin expression in growing antral follicles and corpora lutea of HF dams. Conversely, in both gonads and epididymal WAT of HF offspring, leptin and its receptor were significantly higher expressed compared with BD. Immunolocalization of leptin system in HF offspring gonads showed higher expression in growing and antral follicles of the ovary, seminiferous tubules, and interstitial tissue of testes. In conclusion, high gonadal and gonadal-WAT expression of leptin system was observed in the offspring of dams fed a HF diet during pregnancy and lactation.

Key words

diet - leptin - white adipose tissue - gonad - rat
 

  • References

  • 1 Mercer JG, Hoggard N, Williams L, Lawrence C, Hannah L, Trayhurn P. Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization. FEBS Lett 1996; 387: 113-116
    CrossrefPubMedSearch in Google Scholar
  • 2 Bjørbaek C, Kahn B. Leptin signaling in the central nervous system and the periphery. Recent Prog Horm Res 2004; 59: 305-331
    CrossrefPubMedSearch in Google Scholar
  • 3 Tsoulis M, Chang P, Moore C, Chan K, Gohir W, Petrik J, Vickers M, Connor K, Sloboda D. Maternal high-fat diet-induced loss of fetal oocytes is associated with compromised follicle growth in adult rat offspring. Biol Reprod 2016; 94: 1-11
    CrossrefPubMedSearch in Google Scholar
  • 4 Campos-Silva P, Furriel A, Costa W, Sampaio F, Gregorio B. Metabolic and testicular effects of the long-term administration of different high-fat diets in adult rats. Int Braz J Urol 2015; 41: 569-575
    CrossrefPubMedSearch in Google Scholar
  • 5 Chen H, Simar D, Lambert K, Mercier J, Morris MJ. Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinol 2008; 149: 5348-5356
    CrossrefPubMedSearch in Google Scholar
  • 6 Jacobs S, Teixeira D, Guilherme C, da Rocha C, Aranda B, Reis A, de Souza M, Franci C, Sanvitto G. The impact of maternal consumption of cafeteria diet on reproductive function in the offspring. Physiol Behav 2014; 129: 280-286
    CrossrefPubMedSearch in Google Scholar
  • 7 Gregoraszczuk E, Slupecka M, Wolinski J, Hejmej A, Bilinska B, Fiedor E, Piwnicka N, Rak A. Maternal high-fat diet during pregnancy and lactation had gender difference effect on adiponectin in rat offspring. J Physiol Pharmacol 2016; 67: 543-553
    PubMedSearch in Google Scholar
  • 8 Słupecka M, Romanowicz K, Woliński J. Maternal high-fat diet during pregnancy and lactation influences obestatin and ghrelin concentrations in milk and plasma of Wistar rat dams and their offspring. Int J Endocrinol 2016; 2016: 1-9
    PubMedSearch in Google Scholar
  • 9 Rak A, Drwal E, Wróbel A, Gregoraszczuk EŁ. Resistin is a survival factor for porcine ovarian follicular cells. Reproduction 2015; 150: 343-355
    CrossrefPubMedSearch in Google Scholar
  • 10 Chabrolle C, Tosca L, Dupont J. Regulation of adiponectin and its receptors in rat ovary by human chorionic gonadotrophin treatment and potential involvement of adiponectin in granulosa cell steroidogenesis. Reproduction 2007; 133: 719-731
    CrossrefPubMedSearch in Google Scholar
  • 11 Reverchon M, Cornuau M, Ramé C, Guerif F, Royère D, Dupont J. Chemerin inhibits IGF-1-induced progesterone and estradiol secretion in human granulosa cells. Hum Reprod 2012; 27: 1790-1800
    CrossrefPubMedSearch in Google Scholar
  • 12 Chehab FF, Mounzih K, Lu R, Lim ME. Early onset of reproductive function in normal female mice treated with leptin. Science 1997; 275: 88-90
    CrossrefPubMedSearch in Google Scholar
  • 13 Spicer LJ, Chamberlain CS, Francisco CC. Ovarian action of leptin: effects on insulin-like growth factor-I-stimulated function of granulosa and thecal cells. Endocrine 2000; 12: 53-59
    CrossrefPubMedSearch in Google Scholar
  • 14 Gregoraszczuk EŁ, Wójtowicz AK, Ptak A, Nowak K. In vitro effect of leptin on steroids’ secretion by FSH- and LH-treated porcine small, medium and large preovulatory follicles. Reprod Biol 2003; 3: 227-239
    PubMedSearch in Google Scholar
  • 15 Zachow RJ, Magoffin DA. Direct intraovarian effects of leptin: impairment of the synergistic action of insulin-like growth factor-I on follicle-stimulating hormone-dependent estradiol-17 beta production by rat ovarian granulosa cells. Endocrinology 1997; 138: 847-850
    CrossrefPubMedSearch in Google Scholar
  • 16 Agarwal SK, Vogel K, Weitsman SR, Magoffin D. Leptin antagonizes the insulin-like growth factor-I augmentation of steroidogenesis in granulosa and theca cells of the human ovary. J Clin Endocrinol Metab 1999; 84: 1072-1076
    PubMedSearch in Google Scholar
  • 17 Tena-Sempere M, Pinilla L, González LC, Diéguez C, Casanueva F, Aguilar E. Leptin inhibits testosterone secretion from adult rat testis in vitro. J Endocrinol 1999; 161: 211-218
    CrossrefPubMedSearch in Google Scholar
  • 18 Gonzalez LC, Pinilla L, Tena-Sempere M, Aguilar E. Leptin (116-130) stimulates prolactin and luteinizing hormone secretion in fasted adult male rats. Neuroendocrinology 1999; 70: 213-220
    CrossrefPubMedSearch in Google Scholar
  • 19 Kotula-Balak M, Hejmej A, Kopera I, Lydka M, Bilinska B. Prenatal and neonatal exposure to flutamide affects function of Leydig cells in adult boar. Domest Anim Endocrinol 2012; 42: 142-154
    CrossrefPubMedSearch in Google Scholar
  • 20 Karbaschi R, Sadeghimahalli F, Zardooz H. Maternal high-fat diet inversely affects insulin sensitivity in dams and young adult male rat offspring. J Zhejiang Univ Sci B 2016; 17: 728-732
    CrossrefPubMedSearch in Google Scholar
  • 21 Highman T, Friedman J, Huston L, Wong W, Catalano P. Longitudinal changes in maternal serum leptin concentrations, body composition, and resting metabolic rate in pregnancy. Am J Obstet Gynecol 1998; 178: 1010-1015
    CrossrefPubMedSearch in Google Scholar
  • 22 Mukherjea R, Castonguay T, Douglass L, Moser-Veillon P. Elevated leptin concentrations in pregnancy and lactation: Possible role as a modulator of substrate utilization. Life Sci 1999; 65: 1183-1193
    CrossrefPubMedSearch in Google Scholar
  • 23 Chien E, Hara M, Rouard M, Yano H, Phillippe M, Polonsky K, Bell G. Increase in serum leptin and uterine leptin receptor messenger RNA levels during pregnancy in rats. Biochem Biophys Res Commun 1997; 237: 476-480
    CrossrefPubMedSearch in Google Scholar
  • 24 Clegg D, Gotoh K, Kemp C, Wortman M, Benoit S, Brown L, D'Alessio D, Tso P, Seeley R, Woods S. Consumption of a high-fat diet induces central insulin resistance independent of adiposity. Physiol Behav 2011; 103: 10-16
    CrossrefPubMedSearch in Google Scholar
  • 25 Desai M, Jellyman J, Han G, Beall M, Lane R, Ross M. Maternal obesity and high-fat diet program offspring metabolic syndrome. Am J Obstet Gynecol. 2014; 237: 1-13
    PubMedSearch in Google Scholar
  • 26 Flier J. Clinical review 94: What’s in a name? In search of leptin’s physiologic role. J Clin Endocrinol Metab 1998; 83: 1407-1413
    PubMedSearch in Google Scholar
  • 27 Verdich C, Toubro S, Buemann B, Holst J, Bülow J, Simonsen L, Søndergaard S, Christensen N, Astrup A. Leptin levels are associated with fat oxidation and dietary-induced weight loss in obesity. Obes Res 2001; 9: 452-461
    CrossrefPubMedSearch in Google Scholar
  • 28 Filozof C, Murúa C, Sanchez M, Brailovsky C, Perman M, Gonzalez C, Ravussin E. Low plasma leptin concentration and low rates of fat oxidation in weight-stable post-obese subjects. Obes Res 2000; 8: 205-210
    CrossrefPubMedSearch in Google Scholar
  • 29 Amengual-Cladera E, Lladó I, Proenza A, Gianotti M. High-fat diet feeding induces a depot-dependent response on the pro-inflammatory state and mitochondrial function of gonadal white adipose tissue. Br J Nutr 2013; 109: 413-424
    CrossrefPubMedSearch in Google Scholar
  • 30 Priego T, Sánchez J, Palou A, Pico C. Effect of high-fat diet feeding on leptin receptor expression in white adipose tissue in rats: Depot- and sex-related differential response. Genes Nutr 2009; 4: 151-156
    CrossrefPubMedSearch in Google Scholar
  • 31 Zerani M, Boiti C, Zampini D, Brecchia G, Dall’Aglio C, Ceccarelli P, Gobbetti A. Ob receptor in rabbit ovary and leptin in vitro regulation of corpora lutea. J Endocrinol 2004; 183: 279-288
    CrossrefPubMedSearch in Google Scholar
  • 32 Sohrabi M, Roushandeh A, Alizadeh Z, Vahidinia A, Vahabian M, Hosseini M. Effect of a high fat diet on ovary morphology, in vitro development, in vitro fertilisation rate and oocyte quality in mice. Singapore Med J 2015; 56: 573-579
    CrossrefPubMedSearch in Google Scholar
  • 33 Cordier A, Léveillé P, Dupont C, Tarrade A, Picone O, Larcher T, Dahirel M, Poumerol E, Mandon-Pepin B, Lévy R, Chavatte-Palmer P. Dietary lipid and cholesterol induce ovarian dysfunction and abnormal LH response to stimulation in rabbits. PLoS One 2013; 8: e63101
    CrossrefPubMedSearch in Google Scholar
  • 34 Zhuo Y, Zhou D, Che L, Fang Z, Lin Y, Wu D. Feeding prepubescent gilts a high-fat diet induces molecular changes in the hypothalamus-pituitary-gonadal axis and predicts early timing of puberty. Nutrition 2014; 30: 890-896
    CrossrefPubMedSearch in Google Scholar
  • 35 Almog B, Gold R, Tajima K, Dantes A, Salim K, Rubinstein M, Barkan D, Homburg R, Lessing J, Nevo N, Gertler A, Amsterdam A. Leptin attenuates follicular apoptosis and accelerates the onset of puberty in immature rats. Mol Cell Endocrinol 2001; 183: 179-191
    CrossrefPubMedSearch in Google Scholar
  • 36 Campos-Silva P, Furriel A, Costa W, Sampaio F, Gregorio B. Metabolic and testicular effects of the long-term administration of different high-fat diets in adult rats. Int Braz J Urol 2015; 41: 569-575
    CrossrefPubMedSearch in Google Scholar
  • 37 Tena-Sempere M, Manna P, Zhang F, Pinilla L, González L, Diéguez C, Huhtaniemi I, Aguilar E. Molecular mechanisms of leptin action in adult rat testis: Potential targets for leptin-induced inhibition of steroidogenesis and pattern of leptin receptor messenger ribonucleic acid expression. J Endocrinol 2001; 170: 413-423
    CrossrefPubMedSearch in Google Scholar
  • 38 Kus I, Sarsilmaz M, Canpolat S, Yilmaz B, Kelestimur H, Akpolat N, Ozogul C. Immunohistochemical, histological and ultrastructural evaluation of the effects of leptin on testes in mice. Arch Androl 2005; 51: 395-405
    PubMedSearch in Google Scholar
  • 39 Bellisario V, Berry A, Capoccia S, Raggi C, Panetta P, Branchi I, Piccaro G, Giorgio M, Pelicci P, Cirulli F. Gender-dependent resiliency to stressful and metabolic challenges following prenatal exposure to high-fat diet in the p66(Shc-/) mouse. Front Behav Neurosci 2014; 8: 285
    PubMedSearch in Google Scholar
  • 40 White CL, Purpera M, Morrison C. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol 2009; 296: R1464-R1472
    CrossrefPubMedSearch in Google Scholar