Metabolic programming of puberty: Sexually dimorphic responses to early nutritional challenges

Endocrinology

Volumn 154, Issue 9, 2013, Pages 3387-3400

  Sanchez Garrido M A ^a,b   Castellano, J M ^a,b   Ruiz Pino, F ^a,b   Garcia Galiano, D ^a,b   Manfredi Lozano, M ^a,b   Leon, S ^a,b   Romero Ruiz, A ^a,b   Dieguez C ^a,c   Pinilla, L ^a,b   Tena Sempere, M ^a,b  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b Instituto de Salud Carlos III   (Spain)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MARKER; FOLLITROPIN; GLUCOSE; GONADOTROPIN; INSULIN; LEPTIN; LUTEINIZING HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DELAYED PUBERTY; FEMALE; GLUCOSE BLOOD LEVEL; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; MALE; MALNUTRITION; METABOLISM; NONHUMAN; OVERNUTRITION; PERINATAL PERIOD; PHENOTYPE; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRENATAL PERIOD; PRIORITY JOURNAL; PUBERTY; RAT; SEX DIFFERENCE; WEANING; WEIGHT GAIN;

AGE FACTORS; ANIMALS; BIOLOGICAL MARKERS; BODY WEIGHT; DIET, HIGH-FAT; FEMALE; FETAL DEVELOPMENT; GONADAL DISORDERS; GONADOTROPINS; INSULIN RESISTANCE; LACTATION; MALE; MALNUTRITION; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; OVERNUTRITION; PREGNANCY; RATS; RATS, WISTAR; SEX CHARACTERISTICS; SEXUAL MATURATION;

EID: 84883193123     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2157     Document Type: Article

References (51)

1. Ojeda SR, Skinner MK. Puberty in the rat. In: Neill JD, ed. The Physiology of Reproduction. San Diego: Academic Press/Elsevier; 2006:2061-2126.
2. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev. 2003;24:668-693.
3. Ojeda SR, Lomniczi A, Sandau U, Matagne V. New concepts on the control of the onset of puberty. Endocr Dev. 2010;17:44-51.
4. Tena-Sempere M. Neuroendocrinology of puberty: recent milestones and new challenges. Mol Cell Endocrinol. 2010;324:1-2.
5. Wilson PW, Umpierrez GE. Insulin resistance and pubertal changes. J Clin Endocrinol Metab. 2008;93:2472-2473.
6. Ojeda SR, Dubay C, Lomniczi A, et al. Gene networks and the neuroendocrine regulation of puberty. Mol Cell Endocrinol. 2010; 324:3-11.
7. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev. 2012;92:1235-1316.
8. Fernandez-Fernandez R, Martini AC, Navarro VM, et al. Novel signals for the integration of energy balance and reproduction. Mol Cell Endocrinol. 2006;254-255:127-132.
9. Martos-Moreno GA, Chowen JA, Argente J. Metabolic signals in human puberty: effects of over and undernutrition. Mol Cell Endocrinol. 2010;324:70-81.
10. Castellano JM, Roa J, Luque RM, et al. KiSS-1/kisspeptins and the metabolic control of reproduction: physiologic roles and putative physiopathological implications. Peptides. 2009;30:139-145.
11. Castellano JM, Bentsen AH, Sanchez-Garrido MA, et al. Early metabolic programming of puberty onset: impact of changes in postnatal feeding and rearing conditions on the timing of puberty and development of the hypothalamic kisspeptin system. Endocrinology. 2011;152:3396-3408.
12. Smith JT, Spencer SJ. Preweaning over- and underfeeding alters onset of puberty in the rat without affecting kisspeptin. Biol Reprod. 2012;86:145,141-148.
13. Caron E, Ciofi P, Prevot V, Bouret SG. Alteration in neonatal nutrition causes perturbations in hypothalamic neural circuits controlling reproductive function. J Neurosci. 2012;32:11486-11494.
14. Ibanez L, de Zegher F. Puberty and prenatal growth. Mol Cell Endocrinol. 2006;254-255:22-25.
15. Aksglaede L, Juul A, Olsen LW, Sorensen TI. Age at puberty and the emerging obesity epidemic. PLoS One. 2009;4:e8450.
16. Toppari J, Juul A. Trends in puberty timing in humans and environmental modifiers. Mol Cell Endocrinol. 2010;324:39-44.
17. Lakshman R, Forouhi NG, Sharp SJ, et al. Early age at menarche associated with cardiovascular disease and mortality. J Clin Endocrinol Metab. 2009;94:4953-4960.
18. Widen E, Silventoinen K, Sovio U, et al. Pubertal timing and growth influences cardiometabolic risk factors in adult males and females. Diabetes Care. 2012;35:850-856.
19. Engelbregt MJ, van Weissenbruch MM, Popp-Snijders C, Delemarre-van de Waal HA. Delayed first cycle in intrauterine growth-retarded and postnatally undernourished female rats: follicular growth and ovulation after stimulation with pregnant mare serum gonadotropin at first cycle. J Endocrinol. 2002;173:297-304.
20. van Weissenbruch MM, Engelbregt MJ, Veening MA, Delemarrevan de Waal HA. Fetal nutrition and timing of puberty. Endocr Dev. 2005;8:15-33.
21. Engelbregt MJ, Houdijk ME, Popp-Snijders C, Delemarre-van de Waal HA. The effects of intra-uterine growth retardation and postnatal undernutrition on onset of puberty in male and female rats. Pediatr Res. 2000;48:803-807.
22. 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.
23. Leonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain JC, Dupouy JP. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod. 2003;68:390-400.
24. Iwasa T, Matsuzaki T, Murakami M, et al. Effects of intrauterine undernutrition on hypothalamic Kiss1 expression and the timing of puberty in female rats. J Physiol. 2010;588:821-829.
25. da Silva Faria T, da Fonte Ramos C, Sampaio FJ. Puberty onset in the female offspring of rats submitted to protein or energy restricted diet during lactation. J Nutr Biochem. 2004;15:123-127.
26. Faria Tda S, Brasil Fde B, Sampaio FJ, Ramos Cda F. Maternal malnutrition during lactation alters the folliculogenesis and gonadotropins and estrogen isoforms ovarian receptors in the offspring at puberty. J Endocrinol. 2008;198:625-634.
27. Ibanez L, de Zegher F, Potau N. Anovulation after precocious pubarche: early markers and time course in adolescence. J Clin Endocrinol Metab. 1999;84:2691-2695.
28. Ibanez L, Jimenez R, de Zegher F. Early puberty-menarche after precocious pubarche: relation to prenatal growth. Pediatrics. 2006; 117:117-121.
29. Guzman C, Cabrera R, Cardenas M, Larrea F, Nathanielsz PW, Zambrano E. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol. 2006;572:97-108.
30. Shiell AW, Campbell DM, Hall MH, Barker DJ. Diet in late pregnancy and glucose-insulin metabolism of the offspring 40 years later. BJOG. 2000;107:890-895.
31. Sullivan EL, Smith MS, Grove KL. Perinatal exposure to high-fat diet programs energy balance, metabolism and behavior in adulthood. Neuroendocrinology. 2011;93:1-8.
32. Terasawa E, Kurian JR, Keen KL, Shiel NA, Colman RJ, Capuano SV. Body weight impact on puberty: effects of high-calorie diet on puberty onset in female rhesus monkeys. Endocrinology. 2012;153: 1696-1705.
33. Feng Li X, Lin YS, Kinsey-Jones JS, O'Byrne KT. High-fat diet increases LH pulse frequency and kisspeptin-neurokinin B expression in puberty-advanced female rats. Endocrinology. 2012;153: 4422-4431.
34. Herman-Giddens ME, Steffes J, Harris D, et al. Secondary sexual characteristics in boys: data from the Pediatric Research in Office Settings Network. Pediatrics. 2012;130(5):e1058-e1068.
35. Navarro VM, Fernandez-Fernandez R, Castellano JM, et al. Addoi vanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol. 2004;561:379-386.
36. Navarro VM, Castellano JM, Fernandez-Fernandez R, et al. Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology. 2004;145:4565-4574.
37. Pineda R, Garcia-Galiano D, Roseweir A, et al. Critical roles of kisspeptins in female puberty and preovulatory gonadotropin surges as revealed by a novel antagonist. Endocrinology. 2010;151:722-730.
38. Garcia-Galiano D, Navarro VM, Roa J, et al. The anorexigenic neuropeptide, nesfatin-1, is indispensable for normal puberty onset in the female rat. J Neurosci. 2010;30:7783-7792.
39. Navarro VM, Ruiz-Pino F, Sanchez-Garrido MA, et al. Role of neurokinin B in the control of female puberty and its modulation by metabolic status. J Neurosci. 2012;32:2388-2397.
40. Morris TJ, Vickers M, Gluckman P, Gilmour S, Affara N. Transcriptional profiling of rats subjected to gestational undernourishment: implications for the developmental variations in metabolic traits. PLoS One. 2009;4:e7271.
41. Yura S, Itoh H, Sagawa N, et al. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab. 2005;1:371-378.
42. Plagemann A, Harder T, Rake A, et al. Observations on the orexigenic hypothalamic neuropeptide Y-system in neonatally overfed weanling rats. J Neuroendocrinol. 1999;11:541-546.
43. Lopez M, Seoane LM, Tovar S, et al.Apossible role of neuropeptide Y, agouti-related protein and leptin receptor isoforms in hypothalamic programming by perinatal feeding in the rat. Diabetologia. 2005;48:140-148.
44. Castellano JM, Navarro VM, Fernandez-Fernandez R, et al. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology. 2005;146:3917-3925.
45. Boullu-Ciocca S, Dutour A, Guillaume V, Achard V, Oliver C, Grino M. Postnatal diet-induced obesity in rats upregulates systemic and adipose tissue glucocorticoid metabolism during development and in adulthood: its relationship with the metabolic syndrome. Diabetes. 2005;54:197-203.
46. Quennell JH, Howell CS, Roa J, Augustine RA, Grattan DR, Anderson GM. Leptin deficiency and diet-induced obesity reduce hypothalamic kisspeptin expression in mice. Endocrinology. 2011; 152:1541-1550.
47. Bielohuby M, Menhofer D, Kirchner H, et al. Induction of ketosis in rats fed low-carbohydrate, high-fat diets depends on the relative abundance of dietary fat and protein. Am J Physiol Endocrinol Metab. 2011;300:E65-E76.
48. Bielohuby M, Sawitzky M, Stoehr BJ, et al. Lack of dietary carbohydrates induces hepatic growth hormone (GH) resistance in rats. Endocrinology. 2011;152:1948-1960.
49. Kirk SL, Samuelsson AM, Argenton M, et al. Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS One. 2009;4:e5870.
50. Ozanne SE, Hales CN. Early programming of glucose-insulin metabolism. Trends Endocrinol Metab. 2002;13:368-373.
51. Remmers F, Delemarre-van de Waal HA. Developmental programming of energy balance and its hypothalamic regulation. Endocr Rev. 2011;32:272-311.