Basic nutritional investigationFeeding prepubescent gilts a high-fat diet induces molecular changes in the hypothalamus-pituitary-gonadal axis and predicts early timing of puberty
Introduction
The onset of puberty in females, as measured by the age at menarche, is estimated to have advanced by 6 to 12 mo per 100 y between the 18th and 21st centuries in several northern European countries [1]. This declining age of puberty has been attributed to accelerated growth resulting from improved nutrition, e.g., obese girls tend to mature earlier than normal or thin girls [2], [3], [4]. Thus, the accelerated growth rate due to nutrition fortification seems to be a more important index in predicting the early onset of puberty [5]. Although body condition and the timing of puberty show a strong link in developing girls, the underlying mechanism remains largely unknown.
Puberty is a complex biological process that involves the secretion of gonadotropin-releasing hormone (GnRH) by the hypothalamus, sexual development, adrenal maturation, pubertal development, and gametogenesis. Notably, the secretion of GnRH by the hypothalamus represents the first known step in the reproductive cascade to initiate the activation of pituitary and gonadal function. Therefore, understanding the neuroendocrine control of GnRH secretion may provide insight into the normal reproduction or disorder of the pubertal process. Recently, pharmacologic and genetic studies revealed that GPR54, a G protein-coupled receptor gene, may act as a gatekeeper for normal GnRH physiology and puberty [6]. Kisspeptins, which are encoded by the metastasis suppressor gene Kiss-1, are a natural ligand for GPR54 to elicit a GnRH surge and puberty onset [7], [8]. Kiss-1 and GPR54 may be involved in the early timing of puberty due to accelerated growth. Thus, their gene expression levels represent an interesting research topic.
In the present study, developing gilts were fed an oil-rich diet to induce hormone and molecular changes in the hypothalamus, pituitary, and gonadal tissues. These changes were used to assess whether hormone and molecular changes could predict the early onset of puberty.
Section snippets
Materials and methods
All experimental procedures were approved by the Animal Care and Use Committee of Sichuan Agricultural University.
Age at puberty in gilts
As shown in Table 3, gilts fed HE diets reached puberty 12 d earlier than gilts fed LE diets (P = 0.08). The rate of gilts that reached puberty by age days 180, 190, and 210 in LE and HE gilts were 13% versus 47%, 47% versus 73%, and 93% versus 87%, respectively.
Body weight and back-fat thickness in response to LE and HE diets
As shown in Figures 1 and 2, the body weight and back-fat thickness at P2 point of gilts fed HE diets were significantly higher than those of LE gilts at days 52, 59, 66, and 73 of the experiment (P < 0.01).
Uterus and ovary tissue development in response to LE and HE diets
As shown in Table 4, the
Discussion
Puberty is the process of physical changes by which a child's body matures into an adult body that is capable of fertilization to reproduce offspring. A recent study indicated that girls have entered puberty at increasingly younger ages in the past several decades, and prepubescent obesity is a predictor of early-onset puberty. Therefore, underlying mechanisms that are involved in this process are an interesting subject of study.
In the present study, gilts that consumed extra fat reached
Conclusion
Collectively, the results presented herein suggest that accelerated growth and body fat accumulation induce molecular changes in the Kiss-1/GPR54 system and the hormone secretion, which predict an early onset of puberty.
Acknowledgments
The authors acknowledge the staff in the laboratory for their ongoing assistance.
References (33)
- et al.
Lessons from large population studies on timing and tempo of puberty (secular trends and relation to body size): the European trend
Mol Cell Endocrinol
(2006) GPR54 and puberty
Trends Endocrinol Metab
(2004)- et al.
The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein coupled receptor GPR54
J Biol Chem
(2001) - et al.
Leptin and metabolic control of reproduction
Horm Behav
(2000) - et al.
Influence of obesity on timing of puberty
Int J Androl
(2006) - et al.
Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in office settings network
Pediatrics
(1997) - et al.
Earlier onset of puberty in girls: relation to increased body mass index and race
Pediatrics
(2001) - et al.
Constitutional advancement of growth, a.k.a. early growth acceleration, predicts early puberty and childhood obesity
J Clin Endocrinol Metab
(2010) - et al.
The GPR54 gene as a regulator of puberty
N Engl J Med
(2003) - et al.
Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor
Nature
(2001)
Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates
PNAS
Molecular characterization and estrogen regulation of hypothalamic KISS1 gene in the pig
Biol Reprod
A new mathematical model for relative quantification in real-time RT-PCR
Nucleic Acids Res
Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance and onset
Science
Role of environmental factors in the timing of puberty
Pediatrics
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This work was supported by the National Natural Science Foundation (30871804) of PR China and Program for Changjiang Scholars and Innovative Research Team in University (IRT13083).