Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2010

Open Access 01-12-2010 | Research

Effect of adiponectin on bovine granulosa cell steroidogenesis, oocyte maturation and embryo development

Authors: Virginie Maillard, Svetlana Uzbekova, Florence Guignot, Christine Perreau, Christelle Ramé, Stéphanie Coyral-Castel, Joëlle Dupont

Published in: Reproductive Biology and Endocrinology | Issue 1/2010

Login to get access

Abstract

Background

Adiponectin is an adipokine, mainly produced by adipose tissue. It regulates several reproductive processes. The protein expression of the adiponectin system (adiponectin, its receptors, AdipoR1 and AdipoR2 and the APPL1 adaptor) in bovine ovary and its role on ovarian cells and embryo, remain however to be determined.

Methods

Here, we identified the adiponectin system in bovine ovarian cells and embryo using RT-PCR, immunoblotting and immunohistochemistry. Furthermore, we investigated in vitro the effects of recombinant human adiponectin (10 micro g/mL) on proliferation of granulosa cells (GC) measured by [3H] thymidine incorporation, progesterone and estradiol secretions measured by radioimmunoassay in the culture medium of GC, nuclear oocyte maturation and early embryo development.

Results

We show that the mRNAs and proteins for the adiponectin system are present in bovine ovary (small and large follicles and corpus luteum) and embryo. Adiponectin, AdipoR1 and AdipoR2 were more precisely localized in oocyte, GC and theca cells. Adiponectin increased IGF-1 10(-8) M-induced GC proliferation (P < 0.01) but not basal or insulin 10(-8) M-induced proliferation. Additionally, adiponectin decreased insulin 10(-8) M-induced, but not basal or IGF-1 10(-8) M-induced secretions of progesterone (P < 0.01) and estradiol (P < 0.05) by GC. This decrease in insulin-induced steroidogenesis was associated with a decrease in ERK1/2 MAPK phosphorylation in GC pre-treated with adiponectin. Finally, addition of adiponectin during in vitro maturation affected neither the percentage of oocyte in metaphase-II nor 48-h cleavage and blastocyst day 8 rates.

Conclusions

In bovine species, adiponectin decreased insulin-induced steroidogenesis and increased IGF-1-induced proliferation of cultured GC through a potential involvement of ERK1/2 MAPK pathway, whereas it did not modify oocyte maturation and embryo development in vitro.
Appendix
Available only for authorised users
Literature
1.
Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y: Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 1999, 257: 79-83. 10.1006/bbrc.1999.0255.CrossRefPubMed
2.
Chabrolle C, Tosca L, Dupont J: Regulation of adiponectin and its receptors in rat ovary by human chorionic gonadotrophin treatment and potential involvement of adiponectin in granulosa cell steroidogenesis. Reproduction. 2007, 133: 719-731. 10.1530/REP-06-0244.CrossRefPubMed
3.
Kadowaki T, Yamauchi T: Adiponectin and adiponectin receptors. Endocr Rev. 2005, 26: 439-451. 10.1210/er.2005-0005.CrossRefPubMed
4.
Mitchell M, Armstrong DT, Robker RL, Norman RJ: Adipokines: implications for female fertility and obesity. Reproduction. 2005, 130: 583-597. 10.1530/rep.1.00521.CrossRefPubMed
5.
Ryan AS, Berman DM, Nicklas BJ, Sinha M, Gingerich RL, Meneilly GS, Egan JM, Elahi D: Plasma adiponectin and leptin levels, body composition, and glucose utilization in adult women with wide ranges of age and obesity. Diabetes Care. 2003, 26: 2383-2388. 10.2337/diacare.26.8.2383.CrossRefPubMed
6.
Li S, Shin HJ, Ding EL, van Dam RM: Adiponectin levels and risk of type 2 diabetes: a systematic review and meta-analysis. Jama. 2009, 302: 179-188. 10.1001/jama.2009.976.CrossRefPubMed
7.
Trujillo ME, Scherer PE: Adiponectin--journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J Intern Med. 2005, 257: 167-175. 10.1111/j.1365-2796.2004.01426.x.CrossRefPubMed
8.
Franks S: Polycystic ovary syndrome. N Engl J Med. 1995, 333: 853-861. 10.1056/NEJM199509283331307.CrossRefPubMed
9.
Gambineri A, Pelusi C, Vicennati V, Pagotto U, Pasquali R: Obesity and the polycystic ovary syndrome. Int J Obes Relat Metab Disord. 2002, 26: 883-896. 10.1038/sj.ijo.0801994.CrossRefPubMed
10.
Toulis KA, Goulis DG, Farmakiotis D, Georgopoulos NA, Katsikis I, Tarlatzis BC, Papadimas I, Panidis D: Adiponectin levels in women with polycystic ovary syndrome: a systematic review and a meta-analysis. Hum Reprod Update. 2009, 15: 297-307. 10.1093/humupd/dmp006.CrossRefPubMed
11.
Campos DB, Palin MF, Bordignon V, Murphy BD: The 'beneficial' adipokines in reproduction and fertility. Int J Obes (Lond). 2008, 32: 223-231. 10.1038/sj.ijo.0803719.CrossRef
12.
Combs TP, Pajvani UB, Berg AH, Lin Y, Jelicks LA, Laplante M, Nawrocki AR, Rajala MW, Parlow AF, Cheeseboro L, Ding YY, Russell RG, Lindemann D, Hartley A, Baker GR, Obici S, Deshaies Y, Ludgate M, Rossetti L, Scherer PE: A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology. 2004, 145: 367-383. 10.1210/en.2003-1068.CrossRefPubMed
13.
Ma K, Cabrero A, Saha PK, Kojima H, Li L, Chang BH, Paul A, Chan L: Increased beta -oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J Biol Chem. 2002, 277: 34658-34661. 10.1074/jbc.C200362200.CrossRefPubMed
14.
Maeda N, Shimomura I, Kishida K, Nishizawa H, Matsuda M, Nagaretani H, Furuyama N, Kondo H, Takahashi M, Arita Y, Komuro R, Ouchi N, Kihara S, Tochino Y, Okutomi K, Horie M, Takeda S, Aoyama T, Funahashi T, Matsuzawa Y: Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat Med. 2002, 8: 731-737. 10.1038/nm724.CrossRefPubMed
15.
Chabrolle C, Tosca L, Crochet S, Tesseraud S, Dupont J: Expression of adiponectin and its receptors (AdipoR1 and AdipoR2) in chicken ovary: potential role in ovarian steroidogenesis. Domest Anim Endocrinol. 2007, 33: 480-487. 10.1016/j.domaniend.2006.08.002.CrossRefPubMed
16.
Chabrolle C, Tosca L, Rame C, Lecomte P, Royere D, Dupont J: Adiponectin increases insulin-like growth factor I-induced progesterone and estradiol secretion in human granulosa cells. Fertil Steril. 2009, 92: 1988-1996. 10.1016/j.fertnstert.2008.09.008.CrossRefPubMed
17.
Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R, Kadowaki T: Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature. 2003, 423: 762-769. 10.1038/nature01705.CrossRefPubMed
18.
Tang YT, Hu T, Arterburn M, Boyle B, Bright JM, Emtage PC, Funk WD: PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif. J Mol Evol. 2005, 61: 372-380. 10.1007/s00239-004-0375-2.CrossRefPubMed
19.
Mao X, Kikani CK, Riojas RA, Langlais P, Wang L, Ramos FJ, Fang Q, Christ-Roberts CY, Hong JY, Kim RY, Liu F, Dong LQ: APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat Cell Biol. 2006, 8: 516-523. 10.1038/ncb1404.CrossRefPubMed
20.
Lee MH, Klein RL, El-Shewy HM, Luttrell DK, Luttrell LM: The adiponectin receptors AdipoR1 and AdipoR2 activate ERK1/2 through a Src/Ras-dependent pathway and stimulate cell growth. Biochemistry. 2008, 47: 11682-11692. 10.1021/bi801451f.PubMedCentralCrossRefPubMed
21.
Lord E, Ledoux S, Murphy BD, Beaudry D, Palin MF: Expression of adiponectin and its receptors in swine. J Anim Sci. 2005, 83: 565-578.PubMed
22.
Lagaly DV, Aad PY, Grado-Ahuir JA, Hulsey LB, Spicer LJ: Role of adiponectin in regulating ovarian theca and granulosa cell function. Mol Cell Endocrinol. 2008, 284: 38-45. 10.1016/j.mce.2008.01.007.CrossRefPubMed
23.
Psilopanagioti A, Papadaki H, Kranioti EF, Alexandrides TK, Varakis JN: Expression of adiponectin and adiponectin receptors in human pituitary gland and brain. Neuroendocrinology. 2009, 89: 38-47. 10.1159/000151396.CrossRefPubMed
24.
Archanco M, Gomez-Ambrosi J, Tena-Sempere M, Fruhbeck G, Burrell MA: Expression of leptin and adiponectin in the rat oviduct. J Histochem Cytochem. 2007, 55: 1027-1037. 10.1369/jhc.6A7128.2007.CrossRefPubMed
25.
Schmidt T, Fischer S, Tsikolia N, Navarrete Santos A, Rohrbach S, Ramin N, Thieme R, Fischer B: Expression of adipokines in preimplantation rabbit and mice embryos. Histochem Cell Biol. 2008, 129: 817-825. 10.1007/s00418-008-0409-8.CrossRefPubMed
26.
Caminos JE, Nogueiras R, Gallego R, Bravo S, Tovar S, Garcia-Caballero T, Casanueva FF, Dieguez C: Expression and regulation of adiponectin and receptor in human and rat placenta. J Clin Endocrinol Metab. 2005, 90: 4276-4286. 10.1210/jc.2004-0930.CrossRefPubMed
27.
Royal M, Mann GE, Flint AP: Strategies for reversing the trend towards subfertility in dairy cattle. Vet J. 2000, 160: 53-60. 10.1053/tvjl.1999.0450.CrossRefPubMed
28.
Bauman DE, Currie WB: Partitioning of nutrients during pregnancy and lactation: a review of mechanisms involving homeostasis and homeorhesis. J Dairy Sci. 1980, 63: 1514-1529.CrossRefPubMed
29.
Tamminga S, Luteijn PA, Meijer RGM: Changes in composition and energy content of liveweight loss in dairy cows with time after parturition. Livestock Prod Sci. 1997, 52: 31-38. 10.1016/S0301-6226(97)00115-2.CrossRef
30.
Leroy JL, Opsomer G, Van Soom A, Goovaerts IG, Bols PE: Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part I. The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high-yielding dairy cows. Reprod Domest Anim. 2008, 43: 612-622. 10.1111/j.1439-0531.2007.00960.x.CrossRefPubMed
31.
Wathes DC, Fenwick M, Cheng Z, Bourne N, Llewellyn S, Morris DG, Kenny D, Murphy J, Fitzpatrick R: Influence of negative energy balance on cyclicity and fertility in the high producing dairy cow. Theriogenology. 2007, 68 (Suppl 1): S232-241. 10.1016/j.theriogenology.2007.04.006.CrossRefPubMed
32.
Tabandeh MR, Hosseini A, Saeb M, Kafi M, Saeb S: Changes in the gene expression of adiponectin and adiponectin receptors (AdipoR1 and AdipoR2) in ovarian follicular cells of dairy cow at different stages of development. Theriogenology.
33.
Donnay I, Faerge I, Grondahl C, Verhaeghe B, Sayoud H, Ponderato N, Galli C, Lazzari G: Effect of prematuration, meiosis activating sterol and enriched maturation medium on the nuclear maturation and competence to development of calf oocytes. Theriogenology. 2004, 62: 1093-1107. 10.1016/j.theriogenology.2003.12.019.CrossRefPubMed
34.
Holm P, Booth PJ, Schmidt MH, Greve T, Callesen H: High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology. 1999, 52: 683-700. 10.1016/S0093-691X(99)00162-4.CrossRefPubMed
35.
36.
Tosca L, Chabrolle C, Uzbekova S, Dupont J: Effects of metformin on bovine granulosa cells steroidogenesis: possible involvement of adenosine 5' monophosphate-activated protein kinase (AMPK). Biol Reprod. 2007, 76: 368-378. 10.1095/biolreprod.106.055749.CrossRefPubMed
37.
Chabrolle C, Jeanpierre E, Tosca L, Rame C, Dupont J: Effects of high levels of glucose on the steroidogenesis and the expression of adiponectin receptors in rat ovarian cells. Reprod Biol Endocrinol. 2008, 6: 11-10.1186/1477-7827-6-11.PubMedCentralCrossRefPubMed
38.
Shimada M, Terada T: FSH and LH induce progesterone production and progesterone receptor synthesis in cumulus cells: a requirement for meiotic resumption in porcine oocytes. Mol Hum Reprod. 2002, 8: 612-618. 10.1093/molehr/8.7.612.CrossRefPubMed
39.
Yamashita Y, Shimada M, Okazaki T, Maeda T, Terada T: Production of progesterone from de novo-synthesized cholesterol in cumulus cells and its physiological role during meiotic resumption of porcine oocytes. Biol Reprod. 2003, 68: 1193-1198. 10.1095/biolreprod.102.010934.CrossRefPubMed
40.
Ledoux S, Campos DB, Lopes FL, Dobias-Goff M, Palin MF, Murphy BD: Adiponectin induces periovulatory changes in ovarian follicular cells. Endocrinology. 2006, 147: 5178-5186. 10.1210/en.2006-0679.CrossRefPubMed
41.
Maddineni S, Metzger S, Ocon O, Hendricks G, Ramachandran R: Adiponectin gene is expressed in multiple tissues in the chicken: food deprivation influences adiponectin messenger ribonucleic acid expression. Endocrinology. 2005, 146: 4250-4256. 10.1210/en.2005-0254.CrossRefPubMed
42.
Ramachandran R, Ocon-Grove OM, Metzger SL: Molecular cloning and tissue expression of chicken AdipoR1 and AdipoR2 complementary deoxyribonucleic acids. Domest Anim Endocrinol. 2007, 33: 19-31. 10.1016/j.domaniend.2006.04.004.CrossRefPubMed
43.
Chappaz E, Albornoz MS, Campos D, Che L, Palin MF, Murphy BD, Bordignon V: Adiponectin enhances in vitro development of swine embryos. Domest Anim Endocrinol. 2008, 35: 198-207. 10.1016/j.domaniend.2008.05.007.CrossRefPubMed
44.
Nakayama S, Miyoshi Y, Ishihara H, Noguchi S: Growth-inhibitory effect of adiponectin via adiponectin receptor 1 on human breast cancer cells through inhibition of S-phase entry without inducing apoptosis. Breast Cancer Res Treat. 2008, 112: 405-410. 10.1007/s10549-007-9874-3.CrossRefPubMed
45.
Sugiyama M, Takahashi H, Hosono K, Endo H, Kato S, Yoneda K, Nozaki Y, Fujita K, Yoneda M, Wada K, Nakagama H, Nakajima A: Adiponectin inhibits colorectal cancer cell growth through the AMPK/mTOR pathway. Int J Oncol. 2009, 34: 339-344.PubMed
46.
Williams GA, Wang Y, Callon KE, Watson M, Lin JM, Lam JB, Costa JL, Orpe A, Broom N, Naot D, Reid IR, Cornish J: In vitro and in vivo effects of adiponectin on bone. Endocrinology. 2009, 150: 3603-3610. 10.1210/en.2008-1639.CrossRefPubMed
47.
Spicer LJ, Alpizar E, Echternkamp SE: Effects of insulin, insulin-like growth factor I, and gonadotropins on bovine granulosa cell proliferation, progesterone production, estradiol production, and(or) insulin-like growth factor I production in vitro. J Anim Sci. 1993, 71: 1232-1241.PubMed
48.
Devoto L, Christenson LK, McAllister JM, Makrigiannakis A, Strauss JF: Insulin and insulin-like growth factor-I and -II modulate human granulosa-lutein cell steroidogenesis: enhancement of steroidogenic acute regulatory protein (StAR) expression. Mol Hum Reprod. 1999, 5: 1003-1010. 10.1093/molehr/5.11.1003.CrossRefPubMed
49.
Wu X, Motoshima H, Mahadev K, Stalker TJ, Scalia R, Goldstein BJ: Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes. Diabetes. 2003, 52: 1355-1363. 10.2337/diabetes.52.6.1355.CrossRefPubMed
50.
Moore RK, Otsuka F, Shimasaki S: Role of ERK1/2 in the differential synthesis of progesterone and estradiol by granulosa cells. Biochem Biophys Res Commun. 2001, 289: 796-800. 10.1006/bbrc.2001.6052.CrossRefPubMed
51.
Tosca L, Froment P, Solnais P, Ferre P, Foufelle F, Dupont J: Adenosine 5'-monophosphate-activated protein kinase regulates progesterone secretion in rat granulosa cells. Endocrinology. 2005, 146: 4500-4513. 10.1210/en.2005-0301.CrossRefPubMed
52.
Ryan KE, Glister C, Lonergan P, Martin F, Knight PG, Evans AC: Functional significance of the signal transduction pathways Akt and Erk in ovarian follicles: in vitro and in vivo studies in cattle and sheep. J Ovarian Res. 2008, 1: 2-10.1186/1757-2215-1-2.PubMedCentralCrossRefPubMed
53.
Silva JM, Hamel M, Sahmi M, Price CA: Control of oestradiol secretion and of cytochrome P450 aromatase messenger ribonucleic acid accumulation by FSH involves different intracellular pathways in oestrogenic bovine granulosa cells in vitro. Reproduction. 2006, 132: 909-917. 10.1530/REP-06-0058.CrossRefPubMed
Metadata
Title
Effect of adiponectin on bovine granulosa cell steroidogenesis, oocyte maturation and embryo development
Authors
Virginie Maillard
Svetlana Uzbekova
Florence Guignot
Christine Perreau
Christelle Ramé
Stéphanie Coyral-Castel
Joëlle Dupont
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2010
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-8-23

Other articles of this Issue 1/2010

Reproductive Biology and Endocrinology 1/2010 Go to the issue

Research

Effect of chronic treatment with Rosiglitazone on Leydig cell steroidogenesis in rats: In vivo and ex vivo studies

Research

The expression of syndecan-1, syndecan-4 and decorin in healthy human breast tissue during the menstrual cycle

Research

Estradiol, progesterone, testosterone profiles in human follicular fluid and cultured granulosa cells from luteinized pre-ovulatory follicles

Research

Nuclear factor-kappa B localization and function within intrauterine tissues from term and preterm labor and cultured fetal membranes

Research

Homeobox A7 increases cell proliferation by up-regulation of epidermal growth factor receptor expression in human granulosa cells

Review

Recombinant human follicle-stimulating hormone produces more oocytes with a lower total dose per cycle in assisted reproductive technologies compared with highly purified human menopausal gonadotrophin: a meta-analysis