Feeding prepubescent gilts a high-fat diet induces molecular changes in the hypothalamus-pituitary-gonadal axis and predicts early timing of puberty
Abstract
Objective The onset of puberty in females has been occurring earlier over the past decades, presumably as a result of improved nutrition in developed countries. However, the underlying molecular mechanisms responsible for the early attainment of puberty as a result of nutrition fortification remain largely unknown. The aim of this study was to evaluate the hormone and gene expression changes in prepubescent gilts fed a high-fat diet to investigate whether these changes could predict the early timing of puberty.Methods Forty gilts were fed a daily basal diet (LE) or a basal diet with an additional 270 g/d or 340 g/d of fat (HE) during the prepubescent phase. Blood samples were collected during the prepubescent phase to detect hormone secretion changes in insulin-like growth factor-1, kisspeptin, estradiol, progesterone, and leptin. The gene expressions at the hypothalamus-pituitary-gonadal axis were examined on day 73 of the experiment (average age on day 177) during the prepubescent phase.Results An HE diet resulted in accelerated body weight gain and back-fat thickness at the P2 point compared with LE gilts during the prepubescent phase. Gilts that were fed HE diets attained puberty 12 d earlier than LE gilts, and a larger proportion of HE gilts reached puberty at day 180 or 190 of age. A postmortem analysis revealed a promoted development of the uterus and ovary tissue that was characterized by a 53.7% and 29.5% increase in the uterine and ovary weight, respectively, and an increased length of the uterine horn and oviduct tissue in HE gilts. Real-time quantitative polymerase chain reaction revealed that HE gilts had higher Kiss-1, G protein-coupled receptor 54, gonadotropin-releasing hormone and estrogen receptor α mRNA expression levels in the hypothalamic anteroventral periventricular nucleus; the leptin receptor mRNA expression level was higher in the hypothalamic arcuate nucleus and ovary tissue; the insulin-like growth factor-1 receptor expression was higher in the pituitary and ovary tissues, and the follicle-stimulating hormone and luteinizing hormone mRNA expression levels were higher in the pituitary gland.Conclusion These data showed that the consumption of additional fat can facilitate early attainment of puberty, which can be predicted by the changes in secreted hormones and gene expression in the hypothalamus-pituitary-gonadal axis.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A high-fat diet increases hypothalamic gnrh expression in prepubescent gilts, where this treatment also advances puberty onset, a result observed also in female mice injected with leptin and in obese girls.
“In line with this, a high-fat diet increases hypothalamic gnrh expression in prepubescent gilts (50), where this treatment also advances puberty onset, a result observed also in female mice injected with leptin and in obese girls (50–52).”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in <i>Platynereis</i> (2020) · cites this paper as [50]
Cites
A new mathematical model for relative quantification in real-time RT-PCR
Pfaffl, M. W. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.9.e45 · Cited by 34,610 · see citing works
Weight-Reducing Effects of the Plasma Protein Encoded by the <i>obese</i> Gene
Halaas, J. L., Gajiwala, K. S., Maffei, M., Cohen, S. L., Chait, B. T., Rabinowitz, D., Lallone, R. L., Burley, S. K., & Friedman, J. M. (1995) · Science · doi:10.1126/science.7624777 · Cited by 4,451 · see citing works
The <i>GPR54</i> Gene as a Regulator of Puberty
Seminara, S. B., Messager, S., Chatzidaki, E. E., Thresher, R. R., Acierno, J. S., Shagoury, J. K., Bo-Abbas, Y., Kuohung, W., Schwinof, K. M., Hendrick, A. G., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa035322 · Cited by 2,557 · see citing works
Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54
de Roux, N., Genin, E., Carel, J.-C., Matsuda, F., Chaussain, J.-L., & Milgrom, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1834399100 · Cited by 2,431 · see citing works
Herman-Giddens, M. E., Slora, E. J., Wasserman, R. C., Bourdony, C. J., Bhapkar, M. V., Koch, G. G., & Hasemeier, C. M. (1997) · PEDIATRICS · doi:10.1542/peds.99.4.505 · Cited by 1,709 · see citing works
Kotani, M., Detheux, M., Vandenbogaerde, A., Communi, D., Vanderwinden, J.-M., Le Poul, E., Brézillon, S., Tyldesley, R., Suarez-Huerta, N., Vandeput, F., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104847200 · Cited by 1,546 · see citing works
Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor
Ohtaki, T., Shintani, Y., Honda, S., Matsumoto, H., Hori, A., Kanehashi, K., Terao, Y., Kumano, S., Takatsu, Y., Masuda, Y., et al. (2001) · Nature · doi:10.1038/35079135 · Cited by 1,447 · see citing works
Frisch, R. E., & McArthur, J. W. (1974) · Science · doi:10.1126/science.185.4155.949 · Cited by 1,412 · see citing works
Trophic Action of Leptin on Hypothalamic Neurons That Regulate Feeding
Bouret, S. G., Draper, S. J., & Simerly, R. B. (2004) · Science · doi:10.1126/science.1095004 · Cited by 1,219 · see citing works
Regulation of Kiss1 gene expression in the brain of the female mouse
Smith, J. T., Cunningham, M. J., Rissman, E. F., Clifton, D. K., & Steiner, R. A. (2005) · Endocrinology · doi:10.1210/en.2005-0488 · Cited by 1,102 · see citing works
Increased hypothalamic GPR54 signaling: A potential mechanism for initiation of puberty in primates
Shahab, M., Mastronardi, C. A., Seminara, S. B., Crowley, W. F., Ojeda, S. R., & Plant, T. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409822102 · Cited by 875 · see citing works
Early onset of reproductive function in normal female mice treated with leptin
Chehab, F. F., Mounzih, K., Lu, R., & Lim, M. E. (1997) · Science · doi:10.1126/science.275.5296.88 · Cited by 822 · see citing works
Earlier Onset of Puberty in Girls: Relation to Increased Body Mass Index and Race
Kaplowitz, P. B., Slora, E. J., Wasserman, R. C., Pedlow, S. E., & Herman‐Giddens, M. E. (2001) · PEDIATRICS · doi:10.1542/peds.108.2.347 · Cited by 745 · see citing works
Differential Regulation of KiSS-1 mRNA Expression by Sex Steroids in the Brain of the Male Mouse
Smith, J. T., Lemko, H. M. D., Stoll, E. A., Gottsch, M. L., Braun, R. E., Eacker, S. M., Clifton, D. K., & Steiner, R. A. (2005) · Endocrinology · doi:10.1210/en.2005-0323 · Cited by 694 · see citing works
Kinoshita, M., Tsukamura, H., Adachi, S., Matsui, H., Uenoyama, Y., Iwata, K., Yamada, S., Inoue, K., Ohtaki, T., Matsumoto, H., et al. (2005) · Endocrinology · doi:10.1210/en.2005-0195 · Cited by 507 · see citing works
The Neuroendocrinology of Human Puberty Revisited
Grumbach, M. M. (2002) · Hormone Research in Paediatrics · doi:10.1159/000058094 · Cited by 362 · see citing works
The Estradiol-Induced Surge of Gonadotropin-Releasing Hormone in the Ewe*
Moenter, S. M., Caraty, A., & Karsch, F. J. (1990) · Endocrinology · doi:10.1210/endo-127-3-1375 · Cited by 335 · see citing works
Ong, K. K., Ahmed, M. L., & Dunger, D. B. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2006.04.018 · Cited by 298 · see citing works
Mushroom bodies of the cockroach: Their participation in place memory
Mizunami, M., Weibrecht, J. M., & Strausfeld, N. J. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19981228)402:4 · Cited by 284 · see citing works
Influence of obesity on timing of puberty
BIRO, F. M., KHOURY, P., & MORRISON, J. A. (2006) · International Journal of Andrology · doi:10.1111/j.1365-2605.2005.00602.x · Cited by 241 · see citing works
Role of Environmental Factors in the Timing of Puberty
Euling, S. Y., Selevan, S. G., Pescovitz, O. H., & Skakkebæk, N. E. (2008) · PEDIATRICS · doi:10.1542/peds.2007-1813c · Cited by 222 · see citing works
Neurobiological mechanisms of puberty in higher primates
Plant, T. M. (2004) · Human Reproduction Update · doi:10.1093/humupd/dmh001 · Cited by 187 · see citing works
IGF-1 in the Brain as a Regulator of Reproductive Neuroendocrine Function
Daftary, S. S., & Gore, A. C. (2005) · Experimental Biology and Medicine · doi:10.1177/153537020523000503 · Cited by 181 · see citing works
Hormonal Regulation of Female Reproduction
Christensen, A., Bentley, G., Cabrera, R., Ortega, H. H., Perfito, N., Wu, T. J., & Micevych, P. E. (2012) · Hormone and Metabolic Research · doi:10.1055/s-0032-1306301 · Cited by 159 · see citing works
Tomikawa, J., Uenoyama, Y., Ozawa, M., Fukanuma, T., Takase, K., Goto, T., Abe, H., Ieda, N., Minabe, S., Deura, C., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114245109 · Cited by 150 · see citing works
Molecular Characterization and Estrogen Regulation of Hypothalamic KISS1 Gene in the Pig1
Tomikawa, J., Homma, T., Tajima, S., Shibata, T., Inamoto, Y., Takase, K., Inoue, N., Ohkura, S., Uenoyama, Y., Maeda, K., et al. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.109.079863 · Cited by 126 · see citing works
Leptin and metabolic control of reproduction.
Schneider, J., Zhou, D., & Blum, R. M. (2000) · Hormones and Behavior · doi:10.1006/hbeh.2000.1590 · Cited by 106 · see citing works
Self-citationΚalamatianos, T., Grimshaw, S. E., Poorun, R., Hahn, J. D., & Coen, C. W. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01757.x · Cited by 101 · see citing works
Colledge, W. H. (2004) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2004.09.008 · Cited by 72 · see citing works
Papadimitriou, A., Nicolaidou, P., Fretzayas, A., & Chrousos, G. P. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0895 · Cited by 47 · see citing works
Němcová, L., Nagyová, E., Petlach, M., et al. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.106.057927 · Cited by 45 · see citing works
Sense and Nonsense in Metabolic Control of Reproduction
Schneider, J. E., Klingerman, C. M., & Abdulhay, A. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00026 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Andreatta, G., Broyart, C., Borghgraef, C., Vadiwala, K., Kozin, V., Polo, A., Bileck, A., Beets, I., Schoofs, L., Gerner, C., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1910262116 · Cited by 61 · see citing works
- Authors
- Zhuo, Y., Zhou, D., Che, L., Fang, Z., Lin, Y., & Wu, D.
- Affiliations
- Sichuan Agricultural University (CN)
- Corresponding author
- Wu, De
- Venue
- Nutrition
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 30
- Issue
- 7-8
- Pages
- 890-896
- ISSN
- 0899-9007 (ISSN-L)
- OpenAlex
- W1990637682
- Cited by
- 33
- References
- 32
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 4 · 2020: 2 · 2019: 6 · 2018: 4 · 2017: 5 · 2016: 5 · 2014: 1
- FWCI
- 4.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- high-fat diet, hypothalamic-pituitary-gonadal axis, kisspeptin, kisspeptin receptor, gonadotropin-releasing hormone, estrogen receptor alpha, leptin receptor, IGF-1 receptor, follicle-stimulating hormone, luteinizing hormone, swine reproduction, gene expression, hormone secretion
- MeSH terms
- Adipose Tissue, Animals, Animal Nutritional Physiological Phenomena, Dietary Fats, Female, Hormones, Hypothalamo-Hypophyseal System, Organ Size, Ovary, Puberty, RNA, Messenger, Sexual Maturation, Swine, Uterus, Weight Gain, Diet, High-Fat
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review