Impact of food restriction on the expression of the adiponectin system and genes in the hypothalamic-pituitary-ovarian axis of pre-pubertal ewes
Abstract
Adiponectin, a cytokine secreted typically by adipocytes, has been implicated as a molecular switch between female reproduction and energy balance. The present study was undertaken to investigate the expression of adiponectin system and patterns of genes in the hypothalamic-pituitary-ovary (HPO) axis of food-restricted pre-pubertal ewes. Eighteen 2-month-old female ewes were assigned to 3 groups after a pre-feeding ad libitum for 10 days (six in each group): the control group (C), the low-food-restricted group (LR) and the high-food-restricted group (HR), which were fed with 100%, 70% and 50% of ad libitum food intake, respectively. The hypothalamus, pituitary, ovary and serum were collected after food restriction for 2 months. Results by ELISA showed that food restriction increased serum adiponectin concentrations. Quantitative real-time PCR showed that the gene transcriptions for adiponectin receptor 1 (AdipoR1) and 2 (AdipoR2) were enhanced in the hypothalamic-pituitary-ovarian (HPO) axis, while KISS-1/GPR-54 and gonadotropin-releasing hormone (GnRH) in the hypothalamus and luteinizing hormone β-subunit (LHβ) and follicle-stimulating hormone β-subunit (FSHβ) in the pituitary were reduced after food restriction. Immunohistochemistry results demonstrated that AdipoR1 localized in the oocytes of follicles in the ovary. These results suggest that the alterations in the expression of adiponectin and its receptors in response to food restriction might negatively influence the HPO 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?
Gnrh genes are down-regulated in animals exposed to fasting or food restriction.
“Gnrh genes are down-regulated in animals exposed to fasting or food restriction (45, 46).”
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 [46]
Cites
Adiponectin and Adiponectin Receptors
Kadowaki, T., & Yamauchi, T. (2005) · Endocrine Reviews · doi:10.1210/er.2005-0005 · Cited by 2,634 · see citing works
Adiponectin Expression From Human Adipose Tissue
Kern, P. A., Di Gregorio, G. B., Lu, T., Rassouli, N., & Ranganathan, G. (2003) · Diabetes · doi:10.2337/diabetes.52.7.1779 · Cited by 875 · see citing works
Adiponectin Stimulates AMP-Activated Protein Kinase in the Hypothalamus and Increases Food Intake
Kubota, N., Yano, W., Kubota, T., Yamauchi, T., Itoh, S., Kumagai, H., Kozono, H., Takamoto, I., Okamoto, S., Shiuchi, T., et al. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.06.003 · Cited by 844 · see citing works
Energy balance and reproduction
Schneider, J. E. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.02.007 · Cited by 559 · see citing works
Leptin's Actions on the Reproductive Axis: Perspectives and Mechanisms
Cunningham, M. J., Clifton, D. K., & Steiner, R. A. (1999) · Biology of Reproduction · doi:10.1095/biolreprod60.2.216 · Cited by 531 · see citing works
Adipokines and the Peripheral and Neural Control of Energy Balance
Ahima, R. S., & Lazar, M. A. (2008) · Molecular Endocrinology · doi:10.1210/me.2007-0529 · Cited by 314 · see citing works
Adipokines: implications for female fertility and obesity
Mitchell, M., Armstrong, D. T., Robker, R. L., & Norman, R. J. (2005) · Reproduction · doi:10.1530/rep.1.00521 · Cited by 258 · see citing works
Kos, K., Harte, A. L., da Silva, N. F., Tonchev, A. B., Chaldakov, G., James, S. G., Snead, D. R. J., Hoggart, B., O’Hare, J. P., McTernan, P. G., et al. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1841 · Cited by 234 · see citing works
Cameron, J. L., & Nosbisch, C. (1991) · Endocrinology · doi:10.1210/endo-128-3-1532 · Cited by 229 · see citing works
Regulation of Pituitary Cell Function by Adiponectin
Rodríguez‐Pacheco, F., Martínez‐Fuentes, A. J., Tovar, S. A., Pinilla, L., Tena‐Sempere, M., Diéguez, C., Castano, J. P., & Malagón, M. M. (2006) · Endocrinology · doi:10.1210/en.2006-1019 · Cited by 227 · see citing works
Fontana, R., & Torre, S. D. (2016) · Nutrients · doi:10.3390/nu8020087 · Cited by 218 · see citing works
Role of adiponectin in regulating ovarian theca and granulosa cell function
Lagaly, D. V., Aad, P. Y., Grado-Ahuir, J. A., Hulsey, L. B., & SPICER, L. J. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.01.007 · Cited by 189 · see citing works
Chabrolle, C., Tosca, L., & Dupont, J. (2007) · Reproduction · doi:10.1530/rep-06-0244 · Cited by 186 · see citing works
Expression of Adiponectin and Adiponectin Receptors in Human Pituitary Gland and Brain
Psilopanagioti, A., Papadaki, H. H., Kranioti, E. F., Alexandrides, T. K., & Varakis, J. N. (2008) · Neuroendocrinology · doi:10.1159/000151396 · Cited by 171 · see citing works
Expression of adiponectin and its receptors in swine1,2
Lord, É., Ledoux, S., Murphy, B. D., Beaudry, D., & Palin, M. (2005) · Journal of Animal Science · doi:10.2527/2005.833565x · Cited by 169 · see citing works
AdipoR1 mediates the anorexigenic and insulin/leptin‐like actions of adiponectin in the hypothalamus
Coope, A., Milanski, M., ARAUJO, E. P. D., Tambascia, M. A., Saad, M. J. A., Geloneze, B., & Velloso, L. A. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.03.037 · Cited by 165 · see citing works
Chabrolle, C., Tosca, L., Ramé, C., Lecomte, P., Royère, D., & Dupont, J. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.09.008 · Cited by 160 · see citing works
Expression of Adiponectin Receptors and Its Possible Implication in the Human Endometrium
Takemura, Y., Osuga, Y., Yamauchi, T., Kobayashi, M., Harada, M., Hirata, T., Morimoto, C., Hirota, Y., Yoshino, O., Koga, K., et al. (2006) · Endocrinology · doi:10.1210/en.2005-1510 · Cited by 159 · see citing works
Energy metabolism and fertility—a balance preserved for female health
Torre, S. D., Benedusi, V., Fontana, R., & Maggi, A. C. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.203 · Cited by 158 · see citing works
Lu, M. M., Tang, Q., Olefsky, J. M., Mellon, P. L., & Webster, N. J. G. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0330 · Cited by 148 · see citing works
The ‘beneficial’ adipokines in reproduction and fertility
Campos, D. B., Palin, M., Bordignon, V., & Murphy, B. D. (2007) · International Journal of Obesity · doi:10.1038/sj.ijo.0803719 · Cited by 144 · see citing works
Maillard, V., Uzbekova, S., Guignot, F., Perreau, C., Ramé, C., Coyral-Castel, S., & Dupont, J. (2010) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-8-23 · Cited by 143 · see citing works
Wen, J., Lv, W., Yang, J., Nie, A., Cheng, X., Yang, Y., Ge, Y., Li, X.-Y., & Ning, G. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.04.146 · Cited by 135 · see citing works
Chabrolle, C., Tosca, L., Crochet, S., Tesseraud, S., & Dupont, J. (2006) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2006.08.002 · Cited by 132 · see citing works
Adiponectin, obesity, and cardiovascular disease
Faßhauer, M., Paschke, R., & Stümvoll, M. (2004) · Biochimie · doi:10.1016/j.biochi.2004.09.016 · Cited by 117 · see citing works
Urinary adiponectin excretion is increased in patients with overt diabetic nephropathy
Koshimura, J., Fujita, H., Narita, T., Shimotomai, T., Hosoba, M., Yoshioka, N., Kakei, M., Fujishima, H., & Ito, S. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.02.032 · Cited by 114 · see citing works
Ramachandran, R., Ocón-Grove, O. M., & Metzger, S. L. (2006) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2006.04.004 · Cited by 89 · see citing works
Kile, J. P., Alexander, B. M., Moss, G. E., Hallford, D. M., & Nett, T. M. (1991) · Endocrinology · doi:10.1210/endo-128-2-843 · Cited by 86 · see citing works
Adiponectin enhances in vitro development of swine embryos
Chappaz, E., Albornoz, M. S., Campos, D. B., Che, L., Palin, M., Murphy, B. D., & Bordignon, V. (2008) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2008.05.007 · Cited by 85 · see citing works
Adiponectin and energy homeostasis: consensus and controversy
Dridi, S., & Taouis, M. (2009) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2009.06.003 · Cited by 85 · see citing works
Wen, J., Liu, C., Bi, W., Hu, Y., Chen, Q., Huang, H., Liang, J., Li, L., Lin, L., & Chen, G. (2012) · Journal of Endocrinology · doi:10.1530/joe-12-0054 · Cited by 85 · see citing works
Kawwass, J. F., Summer, R. S., & Kallen, C. B. (2015) · Molecular Human Reproduction · doi:10.1093/molehr/gav025 · Cited by 80 · see citing works
Adiponectin and adiponectin receptors in the mouse preimplantation embryo and uterus
Kim, S. T., Marquard, K. L., Stephens, S. M., Louden, E. D., Allsworth, J. E., & Moley, K. H. (2010) · Human Reproduction · doi:10.1093/humrep/deq292 · Cited by 79 · see citing works
Clarke, I. J. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.02.005 · Cited by 58 · see citing works
Kieżun, M., Maleszka, A., Smolińska, N., Nitkiewicz, A., & Kamiński, T. (2013) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-11-18 · Cited by 45 · see citing works
Expression of Adiponectin and its Receptors in the Porcine Hypothalamus During the Oestrous Cycle
Kamiński, T., Smolińska, N., Maleszka, A., Kieżun, M., Dobrzyń, K., Czerwińśka, J., Szeszko, K., & Nitkiewicz, A. (2014) · Reproduction in Domestic Animals · doi:10.1111/rda.12282 · Cited by 38 · see citing works
Steyn, F. J., Boehme, F., Vargas, E. F. M., Wang, K., Parkington, H. C., Rao, J. R., & Chen, C. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01887.x · Cited by 37 · see citing works
Smolińska, N., Dobrzyń, K., Maleszka, A., Kieżun, M., Szeszko, K., & Kamiński, T. (2014) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2014.02.001 · Cited by 37 · see citing works
Blache, D., Chagas, L. M., & Martin, G. B. (2007) · Reproduction in Domestic Ruminants · doi:10.5661/rdr-vi-123 · Cited by 34 · see citing works
Smolińska, N., Maleszka, A., Dobrzyń, K., Kieżun, M., Szeszko, K., & Kamiński, T. (2014) · Theriogenology · doi:10.1016/j.theriogenology.2014.07.018 · Cited by 31 · see citing works
Maleszka, A., Smolińska, N., Nitkiewicz, A., Kieżun, M., Dobrzyń, K., Czerwińśka, J., Szeszko, K., & Kamiński, T. (2014) · Acta Veterinaria Hungarica · doi:10.1556/avet.2014.007 · Cited by 26 · see citing works
Singh, A. K., & Krishna, A. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.06.027 · Cited by 26 · see citing works
Santos, E. D., Pecquery, R., de Mazancourt, P., & Dieudonné, M. (2012) · Vitamins and hormones · doi:10.1016/b978-0-12-398313-8.00008-7 · Cited by 25 · see citing works
Cao, Z., Li, J., Luo, L., Li, X., Liu, M., Gao, M., Yin, Y., & Luan, X. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0085-1 · Cited by 21 · see citing works
Turyn, J., Korczyńska, J., Presler, M., Stelmańska, E., Goyke, E., & Świerczyński, J. (2008) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-008-9733-5 · Cited by 16 · see citing works
Li, H., Song, H., Huang, M., Nie, H., Wang, Z., & Wang, F. (2014) · Reproduction in Domestic Animals · doi:10.1111/rda.12375 · Cited by 13 · see citing works
Self-citationWang, J. (2012) · AFRICAN JOURNAL OF BIOTECHNOLOGY · doi:10.5897/ajb11.2853 · Cited by 6 · see citing works
Central Regulation of Appetite and Satiety Behavior
Lee, E. B., & Ahima, R. S. (2011) · Springer eBooks · doi:10.1007/978-0-387-92271-3_67 · Cited by 3 · see citing works
Thermal Stress and Adipokines Expression
Preedy, V. R., & Hunter, R. J. (2011) · CRC Press eBooks · doi:10.1201/b11036-23 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Barbe, A., Bongrani, A., Mellouk, N., Estienne, A., Kurowska, P., Grandhaye, J., Elfassy, Y., Lévy, R., Rak, A., Froment, P., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20071526 · Cited by 124 · see citing works
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
Adiponectin: A New Regulator of Female Reproductive System
Dobrzyń, K., Smolińska, N., Kieżun, M., Szeszko, K., Rytelewska, E., Kisielewska, K., Gudelska, M., & Kamiński, T. (2018) · International Journal of Endocrinology · doi:10.1155/2018/7965071 · Cited by 61 · see citing works
Regulation of GnRH pulsatility in ewes
Nestor, C. C., Bedenbaugh, M. N., Hileman, S. M., Coolen, L. M., Lehman, M. N., & Goodman, R. L. (2018) · Reproduction · doi:10.1530/rep-18-0127 · Cited by 59 · see citing works
Adiponectin in male reproduction and infertility
Dutta, S., Sengupta, P., & Biswas, A. (2019) · Asian Pacific Journal of Reproduction · doi:10.4103/2305-0500.268153 · Cited by 22 · see citing works
Merkley, C. M., Shuping, S. L., & Nestor, C. C. (2020) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2020.106469 · Cited by 15 · see citing works
The role of the adiponectin system in acute fasting-impaired mouse ovaries
Han, Y., Zhang, S., Zhuang, H., Fan, S., Yang, J., Zhao, L., Bao, W., Gao, F., Zhang, H., Yuan, Z., et al. (2019) · Reproduction · doi:10.1530/rep-19-0086 · Cited by 8 · see citing works
Li, H., Pei, X., Yu, H., Wang, W., & Mao, D. (2023) · Theriogenology · doi:10.1016/j.theriogenology.2023.11.001 · Cited by 6 · see citing works
Self-citationMetabolic memory determines oviductal gene expression of underfed ewes during early gestation
Fernández-Foren, A., Sosa, C., Abecia, J. A., Meneses, C., & Meikle, A. (2022) · Theriogenology · doi:10.1016/j.theriogenology.2022.12.032 · Cited by 5 · see citing works
Pei, X., Li, H., Yu, H., Wang, W., & Mao, D. (2023) · Cells · doi:10.3390/cells12101393 · Cited by 5 · see citing works
Self-citationZhang, G., Guo, Y., Cheng, C.-Y., El-Samahy, M. A., Tong, R., Gao, X., Deng, K., Wang, F., & Lei, Z. (2020) · Theriogenology · doi:10.1016/j.theriogenology.2020.09.002 · Cited by 4 · see citing works
Self-citationKrasaesub, S., Sukmak, M., Intaravichai, P., Boodde, O., Thanantong, N., & Sajapitak, S. (2022) · Indian Journal of Animal Research · doi:10.18805/ijar.bf-1504 · Cited by 1 · see citing works
Adipose-Specific Cytokines as Modulators of Reproductive Activity
Martínez-Barbitta, M., Biagini, A., Costanzi, E., Maranesi, M., García‐Díez, J., Saraiva, C. M. T., Cenci-Goga, B. T., & Zerani, M. (2025) · Biomedicines · doi:10.3390/biomedicines13123067 · Cited by 1 · see citing works
Tian, Y., Wu, X., Zhang, L., Gong, Y., Kang, X., Tian, Y., & Guo, Y. (2026) · Biomolecules · doi:10.3390/biom16060832 · Cited by 1 · see citing works
Impact of pre-breeding feeding practices on rabbit mammary gland development at mid-pregnancyPreprint
Hue-Beauvais, C., Bébin, K., Robert, R., Gardan‐Salmon, D., Maupin, M., Brun, N., Aujean, E., Jaffrézic, F., Simon, S., Charlier, M., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.17.476562 · Cited by 1 · see citing works
Intaravichai, P., Sajapitak, S., Krasaesub, S., Mongkonwattanaporn, T., & Rukkwamsuk, T. (2021) · The Thai Journal of Veterinary Medicine · doi:10.56808/2985-1130.3176
Barbe, A. (2020) · theses.fr (ABES) · doi:10.70675/a1929a18zc99dz4f74zb8f8z614bf9e123e9
Hernández‐Ortega, K., Bello‐Alvarez, C., Domínguez‐Ordóñez, R., García‐Juárez, M., González‐Flores, O., & Camacho‐Arroyo, I. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106940
- Authors
- Wang, R., Kuang, M., Nie, H., Bai, W., Sun, L., Wang, F., Mao, D., & Wang, Z.
- Affiliations
- Nanjing Agricultural University (CN)
- Corresponding author
- Mao, D
- Wang, Z
- Venue
- Reproduction in Domestic Animals
- Publisher
- Wiley
- Published
- 2016-07-13
- Volume
- 51
- Issue
- 5
- Pages
- 657-664
- ISSN
- 0044-5371 (ISSN-L)
- 0936-6768
- 1439-0531
- OpenAlex
- W2463707531
- Cited by
- 18
- References
- 49
- Citations by year
- 2026: 2 · 2025: 1 · 2023: 2 · 2022: 3 · 2021: 1 · 2020: 3 · 2019: 4 · 2018: 2
- FWCI
- 2.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Reproduction in Domestic Animals (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Jiangsu Key Agricultural Technology Support Program (BE2014330)
- Agroscientific Research in the Public Interest (201303143-06)
- 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
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Keywords
- adiponectin, dietary restriction, hypothalamic-pituitary-ovarian axis, adiponectin receptors, AdipoR1, AdipoR2, gonadotropin-releasing hormone, luteinizing hormone beta subunit, follicle-stimulating hormone beta subunit, energy balance, female reproduction, oocytes
- MeSH terms
- Animals, Energy Intake, Female, Food Deprivation, Follicle Stimulating Hormone, Hypothalamo-Hypophyseal System, Luteinizing Hormone, Gonadotropin-Releasing Hormone, Ovary, RNA, Messenger, Sexual Maturation, Sheep, Gene Expression Regulation, Developmental, Adiponectin, Receptors, Adiponectin, Kisspeptins
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