Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Visfatin and resistin in gonadotroph cells: expression, regulation of LH secretion and signalling pathways

Virginie Maillard A B , Sébastien Elis A , Alice Desmarchais A , Céline Hivelin A , Lionel Lardic A , Didier Lomet A , Svetlana Uzbekova A , Philippe Monget A and Joëlle Dupont A
+ Author Affiliations
- Author Affiliations

A UMR85 PRC, INRA, CNRS, IFCE, Université de Tours, 37380 Nouzilly, France.

B Corresponding author. Email: virginie.maillard@inra.fr

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16301
Submitted: 4 August 2016  Accepted: 21 May 2017   Published online: 4 July 2017

Abstract

Visfatin and resistin appear to interfere with reproduction in the gonads, but their potential action at the hypothalamic–pituitary level is not yet known. The aim of the present study was to investigate the mRNA and protein expression of these adipokines in murine gonadotroph cells and to analyse the effects of different concentrations of recombinant mouse visfatin and resistin (0.01, 0.1, 1 and 10 ng mL-1) on LH secretion and signalling pathways in LβT2 cells and/or in primary female mouse pituitary cells. Both visfatin and resistin mRNA and protein were found in vivo in gonadotroph cells. In contrast with resistin, the primary tissue source of visfatin in the mouse was the skeletal muscle, and not adipose tissue. Visfatin and resistin both decreased LH secretion from LβT2 cells after 24 h exposure of cells (P < 0.03). These results were confirmed for resistin in primary cell culture (P < 0.05). Both visfatin (1 ng mL-1) and resistin (1 ng mL-1) increased AMP-activated protein kinase α phosphorylation in LβT2 cells after 5 or 10 min treatment, up to 60 min (P < 0.04). Extracellular signal-regulated kinase 1/2 phosphorylation was transiently increased only after 5 min resistin (1 ng mL-1) treatment (P < 0.01). In conclusion, visfatin and resistin are expressed in gonadotroph cells and they may affect mouse female fertility by regulating LH secretion at the level of the pituitary.

Additional keywords: adipokine, AMP-activated protein kinase, extracellular signal-regulated kinase, gonadotrophin, myokine, nicotinamide phosphoribosyltransferase (NAMPT), RETN, tissue expression.


References

Akhter, N., Johnson, B. W., Crane, C., Iruthayanathan, M., Zhou, Y. H., Kudo, A., and Childs, G. V. (2007). Anterior pituitary leptin expression changes in different reproductive states: in vitro stimulation by gonadotropin-releasing hormone. J. Histochem. Cytochem. 55, 151–166.
Anterior pituitary leptin expression changes in different reproductive states: in vitro stimulation by gonadotropin-releasing hormone.CrossRef | 1:CAS:528:DC%2BD2sXhtFCgtrs%3D&md5=d81cc2105029894c9c9d7c157fb8ca2aCAS |

Banerjee, R. R., and Lazar, M. A. (2003). Resistin: molecular history and prognosis. J. Mol. Med. 81, 218–226.
Resistin: molecular history and prognosis.CrossRef | 1:CAS:528:DC%2BD3sXivFyhurY%3D&md5=f7f84d64240ff997732f709fcd529128CAS |

Banerjee, R. R., Rangwala, S. M., Shapiro, J. S., Rich, A. S., Rhoades, B., Qi, Y., Wang, J., Rajala, M. W., Pocai, A., Scherer, P. E., Steppan, C. M., Ahima, R. S., Obici, S., Rossetti, L., and Lazar, M. A. (2004). Regulation of fasted blood glucose by resistin. Science 303, 1195–1198.
Regulation of fasted blood glucose by resistin.CrossRef | 1:CAS:528:DC%2BD2cXhsVWgtbk%3D&md5=b3b1c2e24101d7afbf45bd399a73fd01CAS |

Bar-Lev, T. H., Harris, D., Tomic, M., Stojilkovic, S., Blumenfeld, Z., Brown, P., Seger, R., and Naor, Z. (2015). Role of PI4K and PI3K-AKT in ERK1/2 activation by GnRH in the pituitary gonadotropes. Mol. Cell. Endocrinol. 415, 12–23.
Role of PI4K and PI3K-AKT in ERK1/2 activation by GnRH in the pituitary gonadotropes.CrossRef | 1:CAS:528:DC%2BC2MXhsFersbzF&md5=9d21c3de45c90b83ce362235b2aaa5caCAS |

Benomar, Y., Gertler, A., De Lacy, P., Crepin, D., Ould Hamouda, H., Riffault, L., and Taouis, M. (2013). Central resistin overexposure induces insulin resistance through Toll-like receptor 4. Diabetes 62, 102–114.
Central resistin overexposure induces insulin resistance through Toll-like receptor 4.CrossRef | 1:CAS:528:DC%2BC3sXlt1Gktw%3D%3D&md5=58709da74430d5e42d24f053caeeedb6CAS |

Bokarewa, M., Nagaev, I., Dahlberg, L., Smith, U., and Tarkowski, A. (2005). Resistin, an adipokine with potent proinflammatory properties. J. Immunol. 174, 5789–5795.
Resistin, an adipokine with potent proinflammatory properties.CrossRef | 1:CAS:528:DC%2BD2MXjsVeqs78%3D&md5=982690b1ab445fb3b53f05a76d5d2235CAS |

Brown, R., Wiesner, G., Ur, E., and Wilkinson, M. (2005). Pituitary resistin gene expression is upregulated in vitro and in vivo by dexamethasone but is unaffected by rosiglitazone. Neuroendocrinology 81, 41–48.
Pituitary resistin gene expression is upregulated in vitro and in vivo by dexamethasone but is unaffected by rosiglitazone.CrossRef | 1:CAS:528:DC%2BD2MXksVKqtbk%3D&md5=eb7a2eea7170cf8a73da22498a808ef5CAS |

Brown, J. E., Onyango, D. J., Ramanjaneya, M., Conner, A. C., Patel, S. T., Dunmore, S. J., and Randeva, H. S. (2010). Visfatin regulates insulin secretion, insulin receptor signalling and mRNA expression of diabetes-related genes in mouse pancreatic beta-cells. J. Mol. Endocrinol. 44, 171–178.
Visfatin regulates insulin secretion, insulin receptor signalling and mRNA expression of diabetes-related genes in mouse pancreatic beta-cells.CrossRef | 1:CAS:528:DC%2BC3cXkvFKhsbg%3D&md5=72ea6abb25b38a2f711025e4a20cd925CAS |

Buggs, C., Weinberg, F., Kim, E., Wolfe, A., Radovick, S., and Wondisford, F. (2006). Insulin augments GnRH-stimulated LHbeta gene expression by Egr-1. Mol. Cell. Endocrinol. 249, 99–106.
Insulin augments GnRH-stimulated LHbeta gene expression by Egr-1.CrossRef | 1:CAS:528:DC%2BD28XjvVWmtLY%3D&md5=e091d059eb10b3aedc8cb468396bb2a1CAS |

Carbajo-Pérez, E., and Watanabe, Y. G. (1990). Cellular proliferation in the anterior pituitary of the rat during the postnatal period. Cell Tissue Res. 261, 333–338.
Cellular proliferation in the anterior pituitary of the rat during the postnatal period.CrossRef |

Carbajo-Pérez, E., Carbajo, S., Orfao, A., Vicente-Villardón, J. L., and Vázquez, R. (1991). Circadian variation in the distribution of cells throughout the different phases of the cell cycle in the anterior pituitary gland of adult male rats as analysed by flow cytometry. J. Endocrinol. 129, 329–333.
Circadian variation in the distribution of cells throughout the different phases of the cell cycle in the anterior pituitary gland of adult male rats as analysed by flow cytometry.CrossRef |

Chabrolle, C., Jeanpierre, E., Tosca, L., Rame, C., and Dupont, J. (2008). Effects of high levels of glucose on the steroidogenesis and the expression of adiponectin receptors in rat ovarian cells. Reprod. Biol. Endocrinol. 6, 11.
Effects of high levels of glucose on the steroidogenesis and the expression of adiponectin receptors in rat ovarian cells.CrossRef |

Chang, Y. H., Chang, D. M., Lin, K. C., Shin, S. J., and Lee, Y. J. (2011). Visfatin in overweight/obesity, type 2 diabetes mellitus, insulin resistance, metabolic syndrome and cardiovascular diseases: a meta-analysis and systemic review. Diabetes Metab. Res. Rev. 27, 515–527.
Visfatin in overweight/obesity, type 2 diabetes mellitus, insulin resistance, metabolic syndrome and cardiovascular diseases: a meta-analysis and systemic review.CrossRef |

Chen, X., Jia, X., Qiao, J., Guan, Y., and Kang, J. (2013). Adipokines in reproductive function: a link between obesity and polycystic ovary syndrome. J. Mol. Endocrinol. 50, R21–R37.
Adipokines in reproductive function: a link between obesity and polycystic ovary syndrome.CrossRef | 1:CAS:528:DC%2BC3sXmsFeju7g%3D&md5=3630bcf266a3922cf914b86606a70ef8CAS |

Cheng, Q., Dong, W., Qian, L., Wu, J., and Peng, Y. (2011). Visfatin inhibits apoptosis of pancreatic beta-cell line, MIN6, via the mitogen-activated protein kinase/phosphoinositide 3-kinase pathway. J. Mol. Endocrinol. 47, 13–21.
Visfatin inhibits apoptosis of pancreatic beta-cell line, MIN6, via the mitogen-activated protein kinase/phosphoinositide 3-kinase pathway.CrossRef | 1:CAS:528:DC%2BC3MXhtFCisbfP&md5=4047e2c2798af578b4a34f750a035f34CAS |

Choi, K. H., Joo, B. S., Sun, S. T., Park, M. J., Son, J. B., Joo, J. K., and Lee, K. S. (2012). Administration of visfatin during superovulation improves developmental competency of oocytes and fertility potential in aged female mice. Fertil. Steril. 97, 1234–1241.e3.
Administration of visfatin during superovulation improves developmental competency of oocytes and fertility potential in aged female mice.CrossRef | 1:CAS:528:DC%2BC38Xktlequ74%3D&md5=a230b17f44d6f7d2610fcfe4a3f3082bCAS |

Chu, Y., Cui, Q., Feng, G., Song, Z., and Jiang, X. (2009). The expression of resistin in adipose tissues of patients with polycystic ovary syndrome and insulin resistance. J. Huazhong Univ. Sci. Technolog. Med. Sci. 29, 642–645.
The expression of resistin in adipose tissues of patients with polycystic ovary syndrome and insulin resistance.CrossRef | 1:CAS:528:DC%2BD1MXht1GisrjF&md5=32a448512eebe2d92e1abc21dc91c76dCAS |

Crane, C., Akhter, N., Johnson, B. W., Iruthayanathan, M., Syed, F., Kudo, A., Zhou, Y. H., and Childs, G. V. (2007). Fasting and glucose effects on pituitary leptin expression: is leptin a local signal for nutrient status? J. Histochem. Cytochem. 55, 1059–1073.
Fasting and glucose effects on pituitary leptin expression: is leptin a local signal for nutrient status?CrossRef | 1:CAS:528:DC%2BD2sXhtVKqtbvP&md5=8f7ad96f99794ae414d80cf2e368c2acCAS |

D’Ippolito, S., Tersigni, C., Scambia, G., and Di Simone, N. (2012). Adipokines, an adipose tissue and placental product with biological functions during pregnancy. Biofactors 38, 14–23.
Adipokines, an adipose tissue and placental product with biological functions during pregnancy.CrossRef | 1:CAS:528:DC%2BC38Xks1eqtrk%3D&md5=a1313b3888f1a414d009416992dae46bCAS |

Dahl, T. B., Holm, S., Aukrust, P., and Halvorsen, B. (2012). Visfatin/NAMPT: a multifaceted molecule with diverse roles in physiology and pathophysiology. Annu. Rev. Nutr. 32, 229–243.
Visfatin/NAMPT: a multifaceted molecule with diverse roles in physiology and pathophysiology.CrossRef | 1:CAS:528:DC%2BC38XhtlOjsrnN&md5=006bc7a074a810144ebcf42a99f4feb5CAS |

Daquinag, A. C., Zhang, Y., Amaya-Manzanares, F., Simmons, P. J., and Kolonin, M. G. (2011). An isoform of decorin is a resistin receptor on the surface of adipose progenitor cells. Cell Stem Cell 9, 74–86.
An isoform of decorin is a resistin receptor on the surface of adipose progenitor cells.CrossRef | 1:CAS:528:DC%2BC3MXosFansrw%3D&md5=fb7f3ea63961c84b2329a2eb2f560d67CAS |

Denef, C. (2008). Paracrinicity: the story of 30 years of cellular pituitary crosstalk. J. Neuroendocrinol. 20, 1–70.
| 1:CAS:528:DC%2BD1cXhslGltrg%3D&md5=43d99f89d5fd23eb6cdb8ed9827cfef3CAS |

Di Simone, N., Di Nicuolo, F., Sanguinetti, M., Castellani, R., D’Asta, M., Caforio, L., and Caruso, A. (2006). Resistin regulates human choriocarcinoma cell invasive behaviour and endothelial cell angiogenic processes. J. Endocrinol. 189, 691–699.
Resistin regulates human choriocarcinoma cell invasive behaviour and endothelial cell angiogenic processes.CrossRef | 1:CAS:528:DC%2BD28XmtFWju7s%3D&md5=b78e88d4081df46956eb3c9479690597CAS |

Diot, M., Reverchon, M., Rame, C., Baumard, Y., and Dupont, J. (2015). Expression and effect of NAMPT (visfatin) on progesterone secretion in hen granulosa cells. Reproduction 150, 53–63.
Expression and effect of NAMPT (visfatin) on progesterone secretion in hen granulosa cells.CrossRef | 1:CAS:528:DC%2BC2MXhsV2ktL3I&md5=ffcbb80dd6aa1d49fbeb3212bdee9415CAS |

Dupré, S. M., Burt, D. W., Talbot, R., Downing, A., Mouzaki, D., Waddington, D., Malpaux, B., Davis, J. R., Lincoln, G. A., and Loudon, A. S. (2008). Identification of melatonin-regulated genes in the ovine pituitary pars tuberalis, a target site for seasonal hormone control. Endocrinology 149, 5527–5539.
Identification of melatonin-regulated genes in the ovine pituitary pars tuberalis, a target site for seasonal hormone control.CrossRef |

Elis, S., Coyral-Castel, S., Freret, S., Cognié, J., Desmarchais, A., Fatet, A., Rame, C., Briant, E., Maillard, V., and Dupont, J. (2013). Expression of adipokine and lipid metabolism genes in adipose tissue of dairy cows differing in a female fertility quantitative trait locus. J. Dairy Sci. 96, 7591–7602.
Expression of adipokine and lipid metabolism genes in adipose tissue of dairy cows differing in a female fertility quantitative trait locus.CrossRef | 1:CAS:528:DC%2BC3sXhs1WitLrN&md5=925f050f75cc5702b224f48fc6defc96CAS |

Escobar-Morreale, H. F., Villuendas, G., Botella-Carretero, J. I., Alvarez-Blasco, F., Sanchon, R., Luque-Ramirez, M., and San Millan, J. L. (2006). Adiponectin and resistin in PCOS: a clinical, biochemical and molecular genetic study. Hum. Reprod. 21, 2257–2265.
Adiponectin and resistin in PCOS: a clinical, biochemical and molecular genetic study.CrossRef | 1:CAS:528:DC%2BD28XhtVWlt7rI&md5=3f5b5f579fdfe0d724f6f5e832de6184CAS |

Fontana, R., and Torre, S. D. (2016). The deep correlation between energy metabolism and reproduction: a view on the effects of nutrition for women fertility. Nutrients 8, 87.
The deep correlation between energy metabolism and reproduction: a view on the effects of nutrition for women fertility.CrossRef |

Froment, P., Seurin, D., Hembert, S., Levine, J. E., Pisselet, C., Monniaux, D., Binoux, M., and Monget, P. (2002). Reproductive abnormalities in human IGF binding protein-1 transgenic female mice. Endocrinology 143, 1801–1808.
Reproductive abnormalities in human IGF binding protein-1 transgenic female mice.CrossRef | 1:CAS:528:DC%2BD38XjtFOjsLc%3D&md5=9dba5e5f7cc67be69522d2d8db75e418CAS |

Fukuhara, A., Matsuda, M., Nishizawa, M., Segawa, K., Tanaka, M., Kishimoto, K., Matsuki, Y., Murakami, M., Ichisaka, T., Murakami, H., et al. (2005). Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science 307, 426–430.
Visfatin: a protein secreted by visceral fat that mimics the effects of insulin.CrossRef | 1:CAS:528:DC%2BD2MXksFyitw%3D%3D&md5=c13701afb09dc1aa90eafd50b10f38c1CAS |

Guzmán, S., Marin, S., Miranda, A., Selivanov, V. A., Centelles, J. J., Harmancey, R., Smih, F., Turkieh, A., Durocher, Y., Zorzano, A., Rouet, P., and Cascante, M. (2014). 13C metabolic flux analysis shows that resistin impairs the metabolic response to insulin in L6E9 myotubes. BMC Syst. Biol. 8, 109.
13C metabolic flux analysis shows that resistin impairs the metabolic response to insulin in L6E9 myotubes.CrossRef |

Horiguchi, K., Syaidah, R., Fujiwara, K., Tsukada, T., Ramadhani, D., Jindatip, D., Kikuchi, M., and Yashiro, T. (2013). Expression of small leucine-rich proteoglycans in rat anterior pituitary gland. Cell Tissue Res. 351, 207–212.
Expression of small leucine-rich proteoglycans in rat anterior pituitary gland.CrossRef | 1:CAS:528:DC%2BC3sXlt1Gjsg%3D%3D&md5=ed38215e8cd5380701c77c0d4b815da1CAS |

Jurčovičová, J., Štofková, A., Škurlová, M., Baculíková, M., Zórad, S., and Stančíková, M. (2010). Alterations in adipocyte glucose transporter GLUT4 and circulating adiponectin and visfatin in rat adjuvant induced arthritis. Gen. Physiol. Biophys. 29, 79–84.
Alterations in adipocyte glucose transporter GLUT4 and circulating adiponectin and visfatin in rat adjuvant induced arthritis.CrossRef |

Kanasaki, H., Mutiara, S., Oride, A., and Miyazaki, K. (2008). Up-regulation of gonadotropin alpha-subunit gene by phosphatidylinositol 3-kinase inhibitors in clonal gonadotroph cells. Neuroendocrinol. Lett. 29, 529–535.
| 1:CAS:528:DC%2BD1cXht1yis7%2FI&md5=34e631e3cd6382e5e0b829c47078e37eCAS |

Kiezun, M., Smolinska, N., Maleszka, A., Dobrzyn, K., Szeszko, K., and Kaminski, T. (2014). Adiponectin expression in the porcine pituitary during the estrous cycle and its effect on LH and FSH secretion. Am. J. Physiol. Endocrinol. Metab. 307, E1038–E1046.
Adiponectin expression in the porcine pituitary during the estrous cycle and its effect on LH and FSH secretion.CrossRef | 1:CAS:528:DC%2BC2MXptVGmsQ%3D%3D&md5=6d24038375187e91611f25d10be71354CAS |

Kim, H. J., Lee, Y. S., Won, E. H., Chang, I. H., Kim, T. H., Park, E. S., Kim, M. K., Kim, W., and Myung, S. C. (2011). Expression of resistin in the prostate and its stimulatory effect on prostate cancer cell proliferation. BJU Int. 108, E77–E83.
Expression of resistin in the prostate and its stimulatory effect on prostate cancer cell proliferation.CrossRef |

Kim, D. S., Kang, S., Moon, N. R., and Park, S. (2014). Central visfatin potentiates glucose-stimulated insulin secretion and beta-cell mass without increasing serum visfatin levels in diabetic rats. Cytokine 65, 159–166.
Central visfatin potentiates glucose-stimulated insulin secretion and beta-cell mass without increasing serum visfatin levels in diabetic rats.CrossRef | 1:CAS:528:DC%2BC3sXhvFOhsbjP&md5=d7d6c35ee9edaf4419cf1d5a341bbe9fCAS |

Krzysik-Walker, S. M., Ocon-Grove, O. M., Maddineni, S. R., Hendricks, G. L., and Ramachandran, R. (2008). Is visfatin an adipokine or myokine? Evidence for greater visfatin expression in skeletal muscle than visceral fat in chickens. Endocrinology 149, 1543–1550.
Is visfatin an adipokine or myokine? Evidence for greater visfatin expression in skeletal muscle than visceral fat in chickens.CrossRef | 1:CAS:528:DC%2BD1cXktVeru7w%3D&md5=3ee5f0fa7f431325265da4424b27e681CAS |

Lee, S., Lee, H. C., Kwon, Y. W., Lee, S. E., Cho, Y., Kim, J., Lee, S., Kim, J. Y., Lee, J., Yang, H. M., Mook-Jung, I., Nam, K. Y., Chung, J., Lazar, M. A., and Kim, H. S. (2014). Adenylyl cyclase-associated protein 1 is a receptor for human resistin and mediates inflammatory actions of human monocytes. Cell Metab. 19, 484–497.
Adenylyl cyclase-associated protein 1 is a receptor for human resistin and mediates inflammatory actions of human monocytes.CrossRef | 1:CAS:528:DC%2BC2cXjsF2gtLg%3D&md5=9a1085f81dc26468883c3f7ba5b5e733CAS |

Lee, J. O., Kim, N., Lee, H. J., Lee, Y. W., Kim, J. K., Kim, H. I., Lee, S. K., Kim, S. J., Park, S. H., and Kim, H. S. (2015). Visfatin, a novel adipokine, stimulates glucose uptake through the Ca2+-dependent AMPK-p38 MAPK pathway in C2C12 skeletal muscle cells. J. Mol. Endocrinol. 54, 251–262.
Visfatin, a novel adipokine, stimulates glucose uptake through the Ca2+-dependent AMPK-p38 MAPK pathway in C2C12 skeletal muscle cells.CrossRef | 1:CAS:528:DC%2BC2MXhsF2nsrnI&md5=7b64f82719a66cd3266ca1fe01f02d94CAS |

Li, F., Li, Y., Duan, Y., Hu, C. A., Tang, Y., and Yin, Y. (2017). Myokines and adipokines: involvement in the crosstalk between skeletal muscle and adipose tissue. Cytokine Growth Factor Rev. 33, 73–82.
Myokines and adipokines: involvement in the crosstalk between skeletal muscle and adipose tissue.CrossRef | 1:CAS:528:DC%2BC28Xhs1yqt77L&md5=2a035e65db9e35117038a7d2bd455169CAS |

Liu, J., Chi, N., Chen, H., Zhang, J., Bian, Y., Cui, G., and Xiu, C. (2013). Resistin protection against endogenous Abeta neuronal cytotoxicity from mitochondrial pathway. Brain Res. 1523, 77–84.
Resistin protection against endogenous Abeta neuronal cytotoxicity from mitochondrial pathway.CrossRef | 1:CAS:528:DC%2BC3sXhtVWgu7bN&md5=5a7e9ea16b4e1c101b1f2bc3c4d04aebCAS |

Liu, X. Y., Ge, L., and Yu, D. M. (2014). Cloning and expression of visfatin and screening of oligopeptides binding with visfatin. Int. J. Clin. Exp. Med. 7, 4828–4834.

Lovren, F., Pan, Y., Shukla, P. C., Quan, A., Teoh, H., Szmitko, P. E., Peterson, M. D., Gupta, M., Al-Omran, M., and Verma, S. (2009). Visfatin activates eNOS via Akt and MAP kinases and improves endothelial cell function and angiogenesis in vitro and in vivo: translational implications for atherosclerosis. Am. J. Physiol. Endocrinol. Metab. 296, E1440–E1449.
Visfatin activates eNOS via Akt and MAP kinases and improves endothelial cell function and angiogenesis in vitro and in vivo: translational implications for atherosclerosis.CrossRef | 1:CAS:528:DC%2BD1MXnsVCltbs%3D&md5=4ad0b8de4290c34a09a82858cfa1b501CAS |

Lu, M., Tang, Q., Olefsky, J. M., Mellon, P. L., and Webster, N. J. (2008). Adiponectin activates adenosine monophosphate-activated protein kinase and decreases luteinizing hormone secretion in LbetaT2 gonadotropes. Mol. Endocrinol. 22, 760–771.
Adiponectin activates adenosine monophosphate-activated protein kinase and decreases luteinizing hormone secretion in LbetaT2 gonadotropes.CrossRef | 1:CAS:528:DC%2BD1cXis12nsLs%3D&md5=3b3094b2eda03f17bbf1602a3aa3b3e6CAS |

Luo, Z., Zhang, Y., Li, F., He, J., Ding, H., Yan, L., and Cheng, H. (2009). Resistin induces insulin resistance by both AMPK-dependent and AMPK-independent mechanisms in HepG2 cells. Endocrine 36, 60–69.
Resistin induces insulin resistance by both AMPK-dependent and AMPK-independent mechanisms in HepG2 cells.CrossRef | 1:CAS:528:DC%2BD1MXpsFOmsrs%3D&md5=b39d9848c9f853158b4daf8cd3c1514cCAS |

Magni, P., Vettor, R., Pagano, C., Calcagno, A., Beretta, E., Messi, E., Zanisi, M., Martini, L., and Motta, M. (1999). Expression of a leptin receptor in immortalized gonadotropin-releasing hormone-secreting neurons. Endocrinology 140, 1581–1585.
Expression of a leptin receptor in immortalized gonadotropin-releasing hormone-secreting neurons.CrossRef | 1:CAS:528:DyaK1MXitFCrtbg%3D&md5=0c1617862989a54f7f1192d8a822ec0fCAS |

Maillard, V., Uzbekova, S., Guignot, F., Perreau, C., Rame, C., Coyral-Castel, S., and Dupont, J. (2010). Effect of adiponectin on bovine granulosa cell steroidogenesis, oocyte maturation and embryo development. Reprod. Biol. Endocrinol. 8, 23.
Effect of adiponectin on bovine granulosa cell steroidogenesis, oocyte maturation and embryo development.CrossRef |

Maillard, V., Froment, P., Rame, C., Uzbekova, S., Elis, S., and Dupont, J. (2011). Expression and effect of resistin on bovine and rat granulosa cell steroidogenesis and proliferation. Reproduction 141, 467–479.
Expression and effect of resistin on bovine and rat granulosa cell steroidogenesis and proliferation.CrossRef | 1:CAS:528:DC%2BC3MXltlKiur8%3D&md5=4b7c30111115431f300bb7beb2b8a22dCAS |

Manders, E. M. M., Verbeek, F. J., and Aten, J. A. (1993). Measurement of co-localization of objects in dual-colour confocal images. J. Microsc. 169, 375–382.
Measurement of co-localization of objects in dual-colour confocal images.CrossRef |

Morash, B. A., Willkinson, D., Ur, E., and Wilkinson, M. (2002). Resistin expression and regulation in mouse pituitary. FEBS Lett. 526, 26–30.
Resistin expression and regulation in mouse pituitary.CrossRef | 1:CAS:528:DC%2BD38Xms1ygsbc%3D&md5=6af0f0903743f0fac38546531898ae77CAS |

Moschen, A. R., Kaser, A., Enrich, B., Mosheimer, B., Theurl, M., Niederegger, H., and Tilg, H. (2007). Visfatin, an adipocytokine with proinflammatory and immunomodulating properties. J. Immunol. 178, 1748–1758.
Visfatin, an adipocytokine with proinflammatory and immunomodulating properties.CrossRef | 1:CAS:528:DC%2BD2sXntVGlsA%3D%3D&md5=81f0faeb8bf28d15c91d9f1a29c57eedCAS |

Munir, I., Yen, H. W., Baruth, T., Tarkowski, R., Azziz, R., Magoffin, D. A., and Jakimiuk, A. J. (2005). Resistin stimulation of 17alpha-hydroxylase activity in ovarian theca cells in vitro: relevance to polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 90, 4852–4857.
Resistin stimulation of 17alpha-hydroxylase activity in ovarian theca cells in vitro: relevance to polycystic ovary syndrome.CrossRef | 1:CAS:528:DC%2BD2MXnvVWks7Y%3D&md5=976d74adcef5ddab56046b414db6588eCAS |

Nagaev, I., and Smith, U. (2001). Insulin resistance and type 2 diabetes are not related to resistin expression in human fat cells or skeletal muscle. Biochem. Biophys. Res. Commun. 285, 561–564.
Insulin resistance and type 2 diabetes are not related to resistin expression in human fat cells or skeletal muscle.CrossRef | 1:CAS:528:DC%2BD3MXkvFOqsrs%3D&md5=5e290ca590d7f9b92528baf7ef19c357CAS |

Nambiar, V., Vijesh, V. V., Lakshmanan, P., Sukumaran, S., and Suganthi, R. (2016). Association of adiponectin and resistin gene polymorphisms in South Indian women with polycystic ovary syndrome. Eur. J. Obstet. Gynecol. Reprod. Biol. 200, 82–88.
Association of adiponectin and resistin gene polymorphisms in South Indian women with polycystic ovary syndrome.CrossRef | 1:CAS:528:DC%2BC28XjslGnu7w%3D&md5=cff0331e878d7f77ed9e9ca9d735b967CAS |

Naor, Z. (2009). Signaling by G-protein-coupled receptor (GPCR): studies on the GnRH receptor. Front. Neuroendocrinol. 30, 10–29.
Signaling by G-protein-coupled receptor (GPCR): studies on the GnRH receptor.CrossRef | 1:CAS:528:DC%2BD1MXhsVKntQ%3D%3D&md5=400ad39a48eaaa8b79ab9480c4b5939aCAS |

Nogueiras, R., Barreiro, M. L., Caminos, J. E., Gaytán, F., Suominen, J. S., Navarro, V. M., Casanueva, F. F., Aguilar, E., Toppari, J., Diéguez, C., and Tena-Sempere, M. (2004). Novel expression of resistin in rat testis: functional role and regulation by nutritional status and hormonal factors. J. Cell Sci. 117, 3247–3257.
Novel expression of resistin in rat testis: functional role and regulation by nutritional status and hormonal factors.CrossRef | 1:CAS:528:DC%2BD2cXms1ensL8%3D&md5=ef6f49c7cd2024dca70ce93f36f78547CAS |

Odle, A. K., Haney, A., Allensworth-James, M., Akhter, N., and Childs, G. V. (2014). Adipocyte versus pituitary leptin in the regulation of pituitary hormones: somatotropes develop normally in the absence of circulating leptin. Endocrinology 155, 4316–4328.
Adipocyte versus pituitary leptin in the regulation of pituitary hormones: somatotropes develop normally in the absence of circulating leptin.CrossRef |

Ogura, K., Irahara, M., Kiyokawa, M., Tezuka, M., Matsuzaki, T., Yasui, T., Kamada, M., and Aono, T. (2001). Effects of leptin on secretion of LH and FSH from primary cultured female rat pituitary cells. Eur. J. Endocrinol. 144, 653–658.
Effects of leptin on secretion of LH and FSH from primary cultured female rat pituitary cells.CrossRef | 1:CAS:528:DC%2BD3MXkt1Chs7Y%3D&md5=05aba12f1bf231df9257bb77735473f5CAS |

Oishi, Y., Okuda, M., Takahashi, H., Fujii, T., and Morii, S. (1993). Cellular proliferation in the anterior pituitary gland of normal adult rats: influences of sex, estrous cycle, and circadian change. Anat. Rec. 235, 111–120.
Cellular proliferation in the anterior pituitary gland of normal adult rats: influences of sex, estrous cycle, and circadian change.CrossRef | 1:STN:280:DyaK3s7htFGmuw%3D%3D&md5=23463175d162928e2a719840c5e3103cCAS |

Olszanecka-Glinianowicz, M., Kuglin, D., Dabkowska-Huc, A., and Skalba, P. (2011). Serum adiponectin and resistin in relation to insulin resistance and markers of hyperandrogenism in lean and obese women with polycystic ovary syndrome. Eur. J. Obstet. Gynecol. Reprod. Biol. 154, 51–56.
Serum adiponectin and resistin in relation to insulin resistance and markers of hyperandrogenism in lean and obese women with polycystic ovary syndrome.CrossRef | 1:CAS:528:DC%2BC3MXhvV2ktLg%3D&md5=817985a6480e6ef0fc0c295b99476b6bCAS |

Ons, E., Gertler, A., Buyse, J., Lebihan-Duval, E., Bordas, A., Goddeeris, B., and Dridi, S. (2010). Visfatin gene expression in chickens is sex and tissue dependent. Domest. Anim. Endocrinol. 38, 63–74.
Visfatin gene expression in chickens is sex and tissue dependent.CrossRef | 1:CAS:528:DC%2BC3cXosFWi&md5=c376eb9c9eea95065c9b15989f938cffCAS |

Pangaribuan, B., Yusuf, I., Mansyur, M., and Wijaya, A. (2011). Serum adiponectin and resistin in relation to insulin resistance and markers of hyperandrogenism in lean and obese women with polycystic ovary syndrome. Ther. Adv. Endocrinol. Metab. 2, 235–245.
Serum adiponectin and resistin in relation to insulin resistance and markers of hyperandrogenism in lean and obese women with polycystic ovary syndrome.CrossRef | 1:CAS:528:DC%2BC38XivVOktL8%3D&md5=1f83ed6adc05f04bbb653925cae14811CAS |

Park, H.-J., Kim, S.-R., Kim, S. S., Wee, H.-J., Bae, M.-K., Ryu, M. H., and Bae, S.-K. (2014). Visfatin promotes cell and tumor growth by upregulating Notch1 in breast cancer. Oncotarget 5, 5087–5099.
Visfatin promotes cell and tumor growth by upregulating Notch1 in breast cancer.CrossRef |

Pernasetti, F., Vasilyev, V. V., Rosenberg, S. B., Bailey, J. S., Huang, H. J., Miller, W. L., and Mellon, P. L. (2001). Cell-specific transcriptional regulation of follicle-stimulating hormone-beta by activin and gonadotropin-releasing hormone in the LbetaT2 pituitary gonadotrope cell model. Endocrinology 142, 2284–2295.
Cell-specific transcriptional regulation of follicle-stimulating hormone-beta by activin and gonadotropin-releasing hormone in the LbetaT2 pituitary gonadotrope cell model.CrossRef | 1:CAS:528:DC%2BD3MXjvFGgu74%3D&md5=223a43275d69be2d4c4f34dbdbd334d7CAS |

Psilopanagioti, A., Papadaki, H., Kranioti, E. F., Alexandrides, T. K., and Varakis, J. N. (2009). Expression of adiponectin and adiponectin receptors in human pituitary gland and brain. Neuroendocrinology 89, 38–47.
Expression of adiponectin and adiponectin receptors in human pituitary gland and brain.CrossRef | 1:CAS:528:DC%2BD1MXhtFSmsL0%3D&md5=d3e58c6e37b86f71eac001348ac4dcc7CAS |

Razvi, S. S., Richards, J. B., Malik, F., Cromar, K. R., Price, R. E., Bell, C. S., Weng, T., Atkins, C. L., Spencer, C. Y., Cockerill, K. J., Alexander, A. L., Blackburn, M. R., Alcorn, J. L., Haque, I. U., and Johnston, R. A. (2015). Resistin deficiency in mice has no effect on pulmonary responses induced by acute ozone exposure. Am. J. Physiol. Lung Cell. Mol. Physiol. 309, L1174–L1185.
| 1:CAS:528:DC%2BC28Xntl2ks7Y%3D&md5=a317d026816ce9256b6722e673450150CAS |

Reverchon, M., Cornuau, M., Cloix, L., Rame, C., Guerif, F., Royere, D., and Dupont, J. (2013). Visfatin is expressed in human granulosa cells: regulation by metformin through AMPK/SIRT1 pathways and its role in steroidogenesis. Mol. Hum. Reprod. 19, 313–326.
Visfatin is expressed in human granulosa cells: regulation by metformin through AMPK/SIRT1 pathways and its role in steroidogenesis.CrossRef | 1:CAS:528:DC%2BC3sXmtlCht7k%3D&md5=e14f193cd4ff56099dd581b3435a7e1dCAS |

Rodriguez-Pacheco, F., Martinez-Fuentes, A. J., Tovar, S., Pinilla, L., Tena-Sempere, M., Dieguez, C., Castano, J. P., and Malagon, M. M. (2007). Regulation of pituitary cell function by adiponectin. Endocrinology 148, 401–410.
Regulation of pituitary cell function by adiponectin.CrossRef | 1:CAS:528:DC%2BD2sXjsFShsg%3D%3D&md5=50e23c788aa5286e77a17ec684d61948CAS |

Sánchez-Solana, B., Laborda, J., and Baladrón, V. (2012). Mouse resistin modulates adipogenesis and glucose uptake in 3T3-L1 preadipocytes through the ROR1 receptor. Mol. Endocrinol. 26, 110–127.
Mouse resistin modulates adipogenesis and glucose uptake in 3T3-L1 preadipocytes through the ROR1 receptor.CrossRef |

Sarmento-Cabral, A., Peinado, J. R., Halliday, L. C., Malagon, M. M., Castano, J. P., Kineman, R. D., and Luque, R. M. (2017). Adipokines (leptin, adiponectin, resistin) differentially regulate all hormonal cell types in primary anterior pituitary cell cultures from two primate species. Sci. Rep. 7, 43537.
Adipokines (leptin, adiponectin, resistin) differentially regulate all hormonal cell types in primary anterior pituitary cell cultures from two primate species.CrossRef |

Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682.
Fiji: an open-source platform for biological-image analysis.CrossRef | 1:CAS:528:DC%2BC38XhtVKnurbJ&md5=63b94b92bb9f0da66a6ccfd027ffe962CAS |

Schindelin, J., Rueden, C. T., Hiner, M. C., and Eliceiri, K. W. (2015). The ImageJ ecosystem: an open platform for biomedical image analysis. Mol. Reprod. Dev. 82, 518–529.
The ImageJ ecosystem: an open platform for biomedical image analysis.CrossRef | 1:CAS:528:DC%2BC2MXhtFehtr%2FI&md5=781afd65f5d60e298b298c7300b8a98bCAS |

Sharma, S., Morinaga, H., Hwang, V., Fan, W., Fernandez, M. O., Varki, N., Olefsky, J. M., and Webster, N. J. (2013). Free fatty acids induce Lhb mRNA but suppress Fshb mRNA in pituitary LbetaT2 gonadotropes and diet-induced obesity reduces FSH levels in male mice and disrupts the proestrous LH/FSH surge in female mice. Endocrinology 154, 2188–2199.
Free fatty acids induce Lhb mRNA but suppress Fshb mRNA in pituitary LbetaT2 gonadotropes and diet-induced obesity reduces FSH levels in male mice and disrupts the proestrous LH/FSH surge in female mice.CrossRef | 1:CAS:528:DC%2BC3sXotl2hur8%3D&md5=3fc2bd0bca8afe5cefb26548d13db97bCAS |

Singh, A., Suragani, M., and Krishna, A. (2014). Effects of resistin on ovarian folliculogenesis and steroidogenesis in the vespertilionid bat, Scotophilus heathi. Gen. Comp. Endocrinol. 208, 73–84.
Effects of resistin on ovarian folliculogenesis and steroidogenesis in the vespertilionid bat, Scotophilus heathi.CrossRef | 1:CAS:528:DC%2BC2cXhsFylt7jL&md5=b0085576557b044b8abbbd806e3d443bCAS |

Skarra, D. V., and Thackray, V. G. (2015). FOXO1 is regulated by insulin and IGF1 in pituitary gonadotropes. Mol. Cell. Endocrinol. 405, 14–24.
FOXO1 is regulated by insulin and IGF1 in pituitary gonadotropes.CrossRef | 1:CAS:528:DC%2BC2MXisl2rt7w%3D&md5=01dc7abb7982e4560ef21af0e6c9ba61CAS |

Spicer, L. J., Schreiber, N. B., Lagaly, D. V., Aad, P. Y., Douthit, L. B., and Grado-Ahuir, J. A. (2011). Effect of resistin on granulosa and theca cell function in cattle. Anim. Reprod. Sci. 124, 19–27.
Effect of resistin on granulosa and theca cell function in cattle.CrossRef | 1:CAS:528:DC%2BC3MXjvVyjsrs%3D&md5=09cf43aa6516f788db3e973f2c0d709eCAS |

Spritzer, P. M., Lecke, S. B., Satler, F., and Morsch, D. M. (2015). Adipose tissue dysfunction, adipokines, and low-grade chronic inflammation in polycystic ovary syndrome. Reproduction 149, R219–R227.
Adipose tissue dysfunction, adipokines, and low-grade chronic inflammation in polycystic ovary syndrome.CrossRef | 1:CAS:528:DC%2BC2MXhtVCkurzK&md5=fa2c185a39cec50c9a951a3948b93686CAS |

Steppan, C. M., Bailey, S. T., Bhat, S., Brown, E. J., Banerjee, R. R., Wright, C. M., Patel, H. R., Ahima, R. S., and Lazar, M. A. (2001). The hormone resistin links obesity to diabetes. Nature 409, 307–312.
The hormone resistin links obesity to diabetes.CrossRef | 1:CAS:528:DC%2BD3MXms12nsA%3D%3D&md5=10033c1745980c248991da13bc1fa359CAS |

Stofkova, A. (2010). Resistin and visfatin: regulators of insulin sensitivity, inflammation and immunity. Endocr. Regul. 44, 25–36.
Resistin and visfatin: regulators of insulin sensitivity, inflammation and immunity.CrossRef | 1:CAS:528:DC%2BC3cXms1CmtLw%3D&md5=0e9ccd389aa4a37c158aa58db41d00b5CAS |

Sun, Y., Wu, Z., Wei, L., Liu, C., Zhu, S., and Tang, S. (2015). High-visfatin levels in women with polycystic ovary syndrome: evidence from a meta-analysis. Gynecol. Endocrinol. 31, 808–814.
High-visfatin levels in women with polycystic ovary syndrome: evidence from a meta-analysis.CrossRef | 1:CAS:528:DC%2BC28Xht1yluro%3D&md5=82849d4f058211e3731b5385beeb8a67CAS |

Tersigni, C., Di Nicuolo, F., D’Ippolito, S., Veglia, M., Castellucci, M., and Di Simone, N. (2011). Adipokines: new emerging roles in fertility and reproduction. Obstet. Gynecol. Surv. 66, 47–63.
Adipokines: new emerging roles in fertility and reproduction.CrossRef |

The Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group (2004). Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil. Steril. 81, 19–25.
Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome.CrossRef |

Tosca, L., Froment, P., Rame, C., McNeilly, J. R., McNeilly, A. S., Maillard, V., and Dupont, J. (2011). Metformin decreases GnRH- and activin-induced gonadotropin secretion in rat pituitary cells: potential involvement of adenosine 5′ monophosphate-activated protein kinase (PRKA). Biol. Reprod. 84, 351–362.
Metformin decreases GnRH- and activin-induced gonadotropin secretion in rat pituitary cells: potential involvement of adenosine 5′ monophosphate-activated protein kinase (PRKA).CrossRef | 1:CAS:528:DC%2BC3MXhsVeltrc%3D&md5=73c18a7a3521ad585c80b573270d7f80CAS |

Van de Voorde, J., Pauwels, B., Boydens, C., and Decaluwe, K. (2013). Adipocytokines in relation to cardiovascular disease. Metabolism 62, 1513–1521.
Adipocytokines in relation to cardiovascular disease.CrossRef | 1:CAS:528:DC%2BC3sXhtFWktb3I&md5=3253b242daab19f789bbfb897232c454CAS |

Wang, Y., Xie, X., and Zhu, W. (2010). Serum adiponectin and resistin levels in patients with polycystic ovarian syndrome and their clinical implications. J. Huazhong Univ. Sci. Technolog. Med. Sci. 30, 638–642.
Serum adiponectin and resistin levels in patients with polycystic ovarian syndrome and their clinical implications.CrossRef |

Wang, P., Xu, T. Y., Guan, Y. F., Tian, W. W., Viollet, B., Rui, Y. C., Zhai, Q. W., Su, D. F., and Miao, C. Y. (2011). Nicotinamide phosphoribosyltransferase protects against ischemic stroke through SIRT1-dependent adenosine monophosphate-activated kinase pathway. Ann. Neurol. 69, 360–374.
Nicotinamide phosphoribosyltransferase protects against ischemic stroke through SIRT1-dependent adenosine monophosphate-activated kinase pathway.CrossRef | 1:CAS:528:DC%2BC3MXktl2lsLk%3D&md5=cedf0bc9fc0c6f02e11bc9af8fa7b1b8CAS |

Wen, J. P., Lv, W. S., Yang, J., Nie, A. F., Cheng, X. B., Yang, Y., Ge, Y., Li, X. Y., and Ning, G. (2008). Globular adiponectin inhibits GnRH secretion from GT1–7 hypothalamic GnRH neurons by induction of hyperpolarization of membrane potential. Biochem. Biophys. Res. Commun. 371, 756–761.
Globular adiponectin inhibits GnRH secretion from GT1–7 hypothalamic GnRH neurons by induction of hyperpolarization of membrane potential.CrossRef | 1:CAS:528:DC%2BD1cXmsFyrt7o%3D&md5=aeb32283bf864703a0af6fcb6a352ae5CAS |

Wen, J. P., Liu, C., Bi, W. K., Hu, Y. T., Chen, Q., Huang, H., Liang, J. X., Li, L. T., Lin, L. X., and Chen, G. (2012). Adiponectin inhibits KISS1 gene transcription through AMPK and specificity protein-1 in the hypothalamic GT1–7 neurons. J. Endocrinol. 214, 177–189.
Adiponectin inhibits KISS1 gene transcription through AMPK and specificity protein-1 in the hypothalamic GT1–7 neurons.CrossRef | 1:CAS:528:DC%2BC38Xht1CgsbrL&md5=3e2e6fd9411ff99f6b7494a13bc547b2CAS |

Wilda, M., Bachner, D., Just, W., Geerkens, C., Kraus, P., Vogel, W., and Hameister, H. (2000). A comparison of the expression pattern of five genes of the family of small leucine-rich proteoglycans during mouse development. J. Bone Miner. Res. 15, 2187–2196.
A comparison of the expression pattern of five genes of the family of small leucine-rich proteoglycans during mouse development.CrossRef | 1:CAS:528:DC%2BD3cXnvVKltL4%3D&md5=165dba1225fc1e68979edd50a4e6cd90CAS |

Xie, H., Tang, S. Y., Luo, X. H., Huang, J., Cui, R. R., Yuan, L. Q., Zhou, H. D., Wu, X. P., and Liao, E. Y. (2007). Insulin-like effects of visfatin on human osteoblasts. Calcif. Tissue Int. 80, 201–210.
Insulin-like effects of visfatin on human osteoblasts.CrossRef | 1:CAS:528:DC%2BD2sXivVSgtrw%3D&md5=9e17b49f2d15d7dfbcf13a3286a31709CAS |

Xiong, W., Knox, A. J., Xu, M., Kiseljak-Vassiliades, K., Colgan, S. P., Brodsky, K. S., Kleinschmidt-Demasters, B. K., Lillehei, K. O., and Wierman, M. E. (2015). Mammalian Ste20-like kinase 4 promotes pituitary cell proliferation and survival under hypoxia. Mol. Endocrinol. 29, 460–472.
Mammalian Ste20-like kinase 4 promotes pituitary cell proliferation and survival under hypoxia.CrossRef | 1:CAS:528:DC%2BC2MXktF2iurc%3D&md5=7dc793420e47cade088cd14fd94ba2c0CAS |

Yang, D., Caraty, A., and Dupont, J. (2005). Molecular mechanisms involved in LH release by the ovine pituitary cells. Domest. Anim. Endocrinol. 29, 488–507.
Molecular mechanisms involved in LH release by the ovine pituitary cells.CrossRef |



Supplementary MaterialSupplementary Material (55 KB) Export Citation