Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-13T04:08:52.858Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal diet-induced obesity in swine with leptin resistance modifies puberty and pregnancy outputs of the adult offspring

Published online by Cambridge University Press:  16 May 2013

A. Gonzalez-Bulnes ,
S. Astiz ,
R. Sanchez-Sanchez ,
M. Perez-Solana  and
E. Gomez-Fidalgo
A. Gonzalez-Bulnes*
Affiliation:
Department of Animal Reproduction, INIA, Madrid, Spain
S. Astiz
Affiliation:
Department of Animal Reproduction, INIA, Madrid, Spain
R. Sanchez-Sanchez
Affiliation:
Department of Animal Reproduction, INIA, Madrid, Spain
M. Perez-Solana
Affiliation:
Department of Animal Reproduction, INIA, Madrid, Spain
E. Gomez-Fidalgo
Affiliation:
Department of Animal Reproduction, INIA, Madrid, Spain
*
Address for correspondence: A. Gonzalez-Bulnes, Animal Reproduction Department, INIA, Avda. Puerta de Hierro s/n. 28040-Madrid, Spain. Email bulnes@inia.es
Get access Rights & Permissions [Opens in a new window]

Abstract

The assessment of reproductive features (puberty, fertility and prolificacy) in female Iberian pigs indicates that exposition to intrauterine maternal malnutrition, either by deficiency or excess, is associated with juvenile obesity and a significantly earlier age of puberty onset. At adulthood, prenatal exposition to undernutrition affects reproductive outputs by diminishing prolificacy, an effect that was not found in females exposed to prenatal overnutrition.

Keywords

fertilityfoetal programmingnutritionprolificacypubertyswine
Type
Brief Report
Information
Journal of Developmental Origins of Health and Disease , Volume 4 , Issue 4 , August 2013 , pp. 290 - 295
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2013 

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

1.Gluckman, PD, Hanson, MA. Living with the past: evolution, development and patterns of disease. Science. 2004; 305, 1733–1736.CrossRefGoogle ScholarPubMed
2.Gonzalez-Bulnes, A, Ovilo, C. Genetic basis, nutritional challenges and adaptive responses in the prenatal origin of obesity and type-2 diabetes. Current Diabetes Rev. 2012; 8, 144–154.CrossRefGoogle ScholarPubMed
3.Gardner, DS, Lea, RG, Sinclair, KD. Developmental programming of reproduction and fertility: what is the evidence? Animal. 2008; 2, 1128–1134.CrossRefGoogle Scholar
4.Gardner, DS, Ozanne, SE, Sinclair, KD. Effect of the early-life nutritional environment on fecundity and fertility of mammals. Philos Trans R Soc Lond B Biol Sci. 2009; 364, 3419–3427.CrossRefGoogle ScholarPubMed
5.Sloboda, DM, Hickey, M, Hart, R. Reproduction in females: the role of the early life environment. Human Reprod Update. 2011; 17, 210–227.CrossRefGoogle ScholarPubMed
6.Vonnahme, KA, Lemley, CO. Programming the offspring through altered uteroplacental hemodynamics: how maternal environment impacts uterine and umbilical blood flow in cattle, sheep and pigs. Reprod. Fertil Dev. 2011; 24, 97–104.CrossRefGoogle ScholarPubMed
7.McMillen, IC, Adam, CL, Mühlhäusler, BS. Early origins of obesity: programming the appetite regulatory system. J Physiol. 2005; 565, 9–17.CrossRefGoogle ScholarPubMed
8.Gonzalez-Bulnes, A, Pallares, P, Ovilo, C. Ovulation, implantation and placentation in females with obesity and metabolic disorders: life in the balance. Endocr Metab Immune Disord Drug Targets. 2011; 11, 285–301.CrossRefGoogle ScholarPubMed
9.Wu, G, Bazer, FW, Wallace, JM, Spencer, TE. Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci. 2006; 84, 2316–2337.CrossRefGoogle ScholarPubMed
10.Houpt, KA, Houpt, TR, Pond, WG. The pig as a model for the study of obesity and of control of food intake: a review. Yale J Biol Med. 1979; 52, 307–329.Google Scholar
11.Douglas, WR. Of pigs and men and research: a review of applications and analogies of the pig; Sus scrofa; in human medical research. Space Life Sci. 1972; 3, 226–234.Google ScholarPubMed
12.Spurlock, ME, Gabler, NK. The development of porcine models of obesity and the metabolic syndrome. J Nutr. 2008; 138, 397–402.CrossRefGoogle ScholarPubMed
13.Aigner, B, Renner, S, Kessler, B, et al. Transgenic pigs as models for translational biomedical research. J Mol Med (Berl). 2010; 88, 653–664.CrossRefGoogle ScholarPubMed
14.Bähr, A, Wolf, E. Domestic animal models for biomedical research. Reprod Domest Anim. 2012; 47(Suppl 4), 59–71.CrossRefGoogle ScholarPubMed
15.SanCristobal, M, Chevalet, C, Haley, CS, et al.Genetic diversity within and between European pig breeds using microsatellite markers. Anim Genet. 2006; 37, 187–198.CrossRefGoogle ScholarPubMed
16.Ollivier, L. European pig genetic diversity: a mini review. Animal. 2009; 3, 915–924.CrossRefGoogle Scholar
17.Silio, L. Developing Breeding Strategies for Lower Input Animal Production Environments (eds. Galal S, Boyazoglu J, Hammond K), 2000; pp. 511–519. ICAR: Roma.Google Scholar
18.López-Bote, C. Sustained utilization of Iberian pig breed. Meat Sci. 1998; 49, S17–S27.CrossRefGoogle Scholar
19.Nieto, R, Miranda, A, García, MA, Aguilera, JF. The effect of dietary protein content and feeding level on the rate of protein deposition and energy utilization in growing Iberian pigs from 15 to 50 kg body weight. Br J Nutr. 2002; 88, 39–49.CrossRefGoogle ScholarPubMed
20.Ovilo, C, Fernández, A, Noguera, JL, et al.Fine mapping of porcine chromosome 6 QTL and LEPR effects on body composition in multiple generations of an Iberian by Landrace intercross. Genet Res. 2005; 85, 57–67.CrossRefGoogle ScholarPubMed
21.Muñoz, G, Óvilo, C, Silió, L, et al. Single and joint population analyses of two experimental pig crosses to confirm QTL on SSC6 and LEPR effects on fatness and growth traits. J Anim Sci. 2009; 87, 459–468.CrossRefGoogle ScholarPubMed
22.Fernandez-Figares, I, Lachica, M, Nieto, R, Rivera-Ferre, MG, Aguilera, JF. Serum profile of metabolites and hormones in obese (Iberian) and lean (Landrace) growing gilts fed balanced or lysine deficient diets. Livestock Sci. 2007; 110, 73–81.CrossRefGoogle Scholar
23.Myers, MG, Cowley, MA, Münzberg, H. Mechanisms of leptin action and leptin resistance. Ann Rev Physiol. 2008; 70, 537–556.CrossRefGoogle ScholarPubMed
24.Lubis, AR, Widia, F, Soegondo, S, Setiawati, A. The role of SOCS-3 protein in leptin resistance and obesity. Acta Med Indones. 2008; 40, 89–95.Google ScholarPubMed
25.Mizuta, E, Kokubo, Y, Yamanaka, I, et al. Leptin gene and leptin receptor gene polymorphisms are associated with sweet preference and obesity. Hypertension Res. 2008; 31, 1069–1077.CrossRefGoogle ScholarPubMed
26.Torres-Rovira, L, Astiz, S, Caro, A, et al. Diet-induced swine model with obesity/leptin resistance for the study of metabolic syndrome and type 2 diabetes. Sci World J. 2012; Article ID 510149, 8pp.CrossRefGoogle Scholar
27.Torres-Rovira, L, Gonzalez-Añover, P, Astiz, S, et al. Effect of an obesogenic diet during the juvenile period on growth pattern, fatness and metabolic, cardiovascular and reproductive features of swine with obesity/leptin resistance. Endocr Metab Immune Disord Drug Targets. 2012. October 23 [Epub ahead of print].Google Scholar
28.Gonzalez-Bulnes, A, Ovilo, C, Lopez-Bote, CJ, et al. Gender-specific early postnatal catch-up growth after intrauterine growth retardation by food restriction in swine with obesity/leptin resistance. Reproduction. 2012; 44, 269–278.CrossRefGoogle Scholar
29.Ibáñez, L, de Zegher, F. Puberty after prenatal growth restraint. Hormone Res. 2006; 65, 112–115.CrossRefGoogle ScholarPubMed
30.Sloboda, DM, Hart, R, Doherty, DA, Pennell, CE, Hickey, M. Age at menarche: influences of prenatal and postnatal growth. J Clin Endocrinol Metabol. 2007; 92, 46–50.CrossRefGoogle ScholarPubMed
31.Hernández, MI, Mericq, V. Impact of being born small for gestational age on onset and progression of puberty. Best Pract Res Clin Endocrinol Metab. 2008; 22, 463–476.CrossRefGoogle ScholarPubMed
32.Sloboda, DM, Howie, GJ, Pleasants, A, Gluckman, PD, Vickers, MH. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One. 2009; 4, e6744.CrossRefGoogle ScholarPubMed
33.McLaren, A. Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol. 2000; 163, 3–9.CrossRefGoogle ScholarPubMed
34.Pepling, ME, Spradling, AC. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol. 2001; 34, 339–351.CrossRefGoogle Scholar
35.Padmanabhan, V, Veiga-Lopez, A, Abbott, DH, Dumesic, DA. Developmental programming of ovarian dysfunction. In Novel Concepts in Ovarian Endocrinology (ed. Gonzalez-Bulnes A), 2007; pp. 1–24. India: Research Signpost Editors: Kerala.Google Scholar
36.Gonzalez-Bulnes, A, Pallares, P, Ovilo, C. Ovulation, implantation and placentation in females with obesity and metabolic disorders: life in the balance. Endocr Metab Immune Disord Drug Targets. 2011; 11, 285–301.CrossRefGoogle ScholarPubMed
37.Kaplowitz, PB. Link between body fat and the timing of puberty. Pediatrics. 2008; 121, S208–S217.CrossRefGoogle ScholarPubMed
38.Slyper, AH. Childhood obesity, adipose tissue distribution, and the pediatric practitioner. Pediatrics. 1998; 102, e4.CrossRefGoogle ScholarPubMed
39.Popovic, V, Casanueva, FF. Leptin; nutrition and reproduction: new insights. Hormones. 2002; 1, 204–220.CrossRefGoogle ScholarPubMed
40.Imakawa, K, Kittock, RJ, Kinder, JE. The influence of dietary energy intake on progesterone concentrations in beef heifers. J Anim Sci. 1983; 6, 454–459.CrossRefGoogle Scholar
41.Frisch, RE. Body fat, puberty and fertility. Biol Rev. 1984; 59, 161–188.CrossRefGoogle ScholarPubMed
42.Barb, CR, Kraeling, RR, Rampacek, GB. Metabolic regulation of the neuroendocrine axis in pigs. Reproduction Suppl. 2002; 59, 203–217.Google ScholarPubMed
43.Barb, CR, Kraeling, RR. Role of leptin in the regulation of gonadotrophin secretion in farm animals. Anim Reprod Sci. 2004; 82–83, 155–167.CrossRefGoogle ScholarPubMed
44.Jasik, CB, Lustig, RH. Adolescent obesity and puberty: the “perfect storm”. Ann NY Acad Sci. 2008; 1135, 265–279.CrossRefGoogle ScholarPubMed
45.Ahmed, ML, Ong, KK, Dunger, DB. Childhood obesity and the timing of puberty. Trends Endocrinol Metab. 2009; 20, 237–242.CrossRefGoogle ScholarPubMed
46.Lumey, LH. Reproductive outcomes in women prenatally exposed to undernutrition: a review of findings from the Dutch famine birth cohort. Proc Nutr Soc. 1998; 57, 129–135.CrossRefGoogle ScholarPubMed
47.Painter, RC, Westendorp, RGJ, de Rooij, SR, et al. Increased reproductive success of women after prenatal undernutrition. Human Reprod. 2008; 23, 2591–2595.CrossRefGoogle ScholarPubMed
48.Dupont, C, Cordier, AG, Junien, C, et al. Maternal environment and the reproductive function of the offspring. Theriogenology. 2012; 78, 1405–1414.CrossRefGoogle ScholarPubMed
49.Meikle, D, Westberg, M. Maternal nutrition and reproduction of daughters in wild house mice (Mus musculus). Reproduction. 2001; 122, 437–442.CrossRefGoogle ScholarPubMed
50.Bernal, AB, Vickers, MH, Hampton, MB, Poynton, RA, Sloboda, DM. Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One. 2010; 5, e15558.CrossRefGoogle ScholarPubMed
51.Rae, MT, Kyle, CE, Miller, DW, et al. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci. 2002; 72, 63–71.CrossRefGoogle ScholarPubMed
52.Kotsampasi, B, Chadio, S, Papadomichelakis, G, et al. Effects of maternal undernutrition on the hypothalamic-pituitary-gonadal axis function in female sheep offspring. Reprod Domest Anim. 2009; 44, 677–684.CrossRefGoogle ScholarPubMed