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

Follicular fluid leptin concentrations and expression of leptin and leptin receptor in the equine ovary and in vitro-matured oocyte with reference to pubertal development and breeds

Anna Lange-Consiglio A , Silvana Arrighi B , Nadia Fiandanese C , Paola Pocar C , Marina Aralla B E , GiamPaolo Bosi B , Vitaliano Borromeo C , Anna Berrini C , Aurora Meucci A , Maria E. Dell’Aquila D and Fausto Cremonesi A F
+ Author Affiliations
- Author Affiliations

A Large Animal Hospital, Reproduction Unit, Università degli Studi di Milano, Via dell’Università, 6, Lodi, 26900, Italy.

B Department of Health, Animal Science and Food Safety, Università degli Studi di Milano, Via Trentacoste, 2, 20133, Italy.

C Department of Veterinary Science and Public Health, Università degli Studi di Milano, Via Celoria, 10, 20133, Italy.

D Department of Animal Production, Università degli Studi di Bari, Strada Casamassima, km 2, 70010, Italy.

E Present address: Ospedale Veterinario San Michele, Via 1° Maggio 37, Tavazzano con Villavesco (LO), 26838, Italy.

F Corresponding author. Email: fausto.cremonesi@unimi.it

Reproduction, Fertility and Development 25(5) 837-846 https://doi.org/10.1071/RD12188
Submitted: 14 June 2012  Accepted: 18 July 2012   Published: 29 August 2012

Abstract

There is no published information about follicular-fluid leptin concentrations or the presence of leptin and leptin receptor in the equine ovary or oocyte. Three groups of mares – adult draft mares, draft fillies and adult Standardbred mares – were included in the study. Leptin and leptin receptor were detected in all immature oocytes by immunofluorescence with higher intensity in oocytes from draft mares compared with draft fillies and Standardbred mares. After in vitro maturation a higher proportion of oocytes reached metaphase II in draft mares than in draft fillies and Standardbred mares, and in all groups both leptin and leptin receptor became localised in the oocyte cortex but with higher immunopositivity in draft mares compared with draft fillies and Standardbred mares. These intensities were confirmed by the expression profiles of leptin and leptin receptor mRNA. Moreover, leptin was detected in ovarian blood vessels in all three types of animal and within the corpora lutea in adult mares. Serum and follicular-fluid concentrations of leptin were similar in draft and Standardbred mares but higher in draft mares than in draft fillies. This study supports the hypothesis that expression of leptin and leptin receptor mRNA and the rate of maturation can be related either to adiposity or to puberty.

Additional keywords: adiposity, mare, puberty.


References

Adamiak, S. J., Mackie, K., Watt, R. G., Webb, R., and Sinclair, K. D. (2005). Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinemia in cattle. Biol. Reprod. 73, 918–926.
Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinemia in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGktb7L&md5=798102f1a8de31a64d412bad3da83ec8CAS | 15972884PubMed |

Baka, S., and Malamitsi-Puchner, A. (2006). Novel follicular fluid factors influencing oocyte developmental potential in IVF: a review. Reprod. Biomed. Online 12, 500–506.
Novel follicular fluid factors influencing oocyte developmental potential in IVF: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktFarsr8%3D&md5=e6050adae6e23ce5a5fb0449f1740b36CAS | 16740225PubMed |

Banks, W. A. (2004). The many lives of leptin. Peptides 25, 331–338.
The many lives of leptin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVagtL0%3D&md5=af333af1707449f32052798e0a0f86d9CAS | 15134858PubMed |

Barr, V. A., Lane, K., and Taylor, S. I. (1999). Subcellular localization and internalization of the four human leptin receptor isoforms. J. Biol. Chem. 274, 21 416–21 424.
Subcellular localization and internalization of the four human leptin receptor isoforms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvVKrtLo%3D&md5=9691e8f40fcd98eac1afd2912438eb1cCAS |

Bouloumié, A., Drexler, H. C., Lafontan, M., and Busse, R. (1998). Leptin, the product of Ob gene, promotes angiogenesis. Circ. Res. 83, 1059–1066.
Leptin, the product of Ob gene, promotes angiogenesis.Crossref | GoogleScholarGoogle Scholar | 9815153PubMed |

Buff, P. R., Dodds, A. C., Morrison, C. D., Whitley, N. C., McFadin, E. L., Daniel, J. A., Djiane, J., and Keisler, D. H. (2002). Leptin in horses: tissue localization and relationship between peripheral concentrations of leptin and body condition. J. Anim. Sci. 80, 2942–2948.
| 1:CAS:528:DC%2BD38XoslKgtLo%3D&md5=d38a2d283d2ea469832fe5adeb79675dCAS | 12462262PubMed |

Craig, J., Zhu, H., Dyce, P. W., Petrik, J., and Li, J. (2004). Leptin enhances oocyte nuclear and cytoplasmic maturation via the mitogen-activated protein kinase pathway. Endocrinology 145, 5355–5363.
Leptin enhances oocyte nuclear and cytoplasmic maturation via the mitogen-activated protein kinase pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVygs7o%3D&md5=79ebe9b8aac9752bfeec6dcf79f735b6CAS | 15284194PubMed |

Cunningham, M. J., Clifton, D. K., and Steiner, R. A. (1999). Leptin’s actions on the reproductive axis: perspectives and mechanisms. Biol. Reprod. 60, 216–222.
Leptin’s actions on the reproductive axis: perspectives and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotlyjtQ%3D%3D&md5=6e99f28b71a683a3022ef19b061ddcc9CAS | 9915984PubMed |

De Placido, G., Alviggi, C., Clarizia, R., Mollo, A., Alviggi, E., Strina, I., Fiore, E., Wilding, M., Pagano, T., and Matarese, G. (2006). Intra-follicular leptin concentration as a predictive factor for in vitro oocyte fertilization in assisted reproductive techniques. J. Endocrinol. Invest. 29, 719–726.
| 1:CAS:528:DC%2BD28XhtlajsbnF&md5=2afaa8e8dc812635165db2a35e73493dCAS | 17033261PubMed |

Driancourt, M. A. (1979). Follicular kinetics in the mare ovary. Ann. Biol. Anim. Bioch. 19, 1443–1453.
Follicular kinetics in the mare ovary.Crossref | GoogleScholarGoogle Scholar |

Ferguson, E. M., Ashworth, C. J., Edwards, S. A., Hawkins, N., Hepburn, N., and Hunter, M. G. (2003). Effect of different nutritional regimens before ovulation on plasma concentrations of metabolic and reproductive hormones and oocyte maturation in gilts. Reproduction 126, 61–71.
Effect of different nutritional regimens before ovulation on plasma concentrations of metabolic and reproductive hormones and oocyte maturation in gilts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvFCnurw%3D&md5=daa728526d2c1adcb640699acd812f78CAS | 12814348PubMed |

Ferreira-Dias, G., Claudino, F., Carvalho, H., Agrícola, R., Alpoim-Moreira, J., and Robalo Silva, J. (2005). Seasonal reproduction in the mare: possible role of plasma leptin, body weight and immune status. Domest. Anim. Endocrinol. 29, 203–213.
Seasonal reproduction in the mare: possible role of plasma leptin, body weight and immune status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVehu7g%3D&md5=ef0f70a86df89403b8e9585cc66f13adCAS | 15927774PubMed |

Fitzgerald, B. P., and McManus, C. J. (2000). Photoperiodic versus metabolic signals as determinants of seasonal anoestrus in the mare. Biol. Reprod. 63, 335–340.
Photoperiodic versus metabolic signals as determinants of seasonal anoestrus in the mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktl2rsbY%3D&md5=a0042df103814744319ba20c51e37ec4CAS | 10859276PubMed |

Fitzgerald, B. P., Reedy, S. E., Sessions, D. R., Powell, D. M., and McManus, C. J. (2002). Potential signals mediating the maintenance of reproductive activity during the non-breeding season of the mare. Reprod. Suppl. 59, 115–129.
| 1:CAS:528:DC%2BD38XmsVajsrk%3D&md5=8a20c8dff2582e09f8d9290c736d5a2eCAS | 12698977PubMed |

Frühbeck, G. (2001). A heliocentric view of leptin. Proc. Nutr. Soc. 60, 301–318.
A heliocentric view of leptin.Crossref | GoogleScholarGoogle Scholar | 11681805PubMed |

Frühbeck, G., Jebb, S. A., and Prentice, A. M. (1998). Leptin: physiology and pathophysiology. Clin. Physiol. 18, 399–419.
Leptin: physiology and pathophysiology.Crossref | GoogleScholarGoogle Scholar | 9784936PubMed |

García-López, M. J., Martínez-Martos, J. M., Mayas, M. D., Carrera, M. P., and Ramírez-Expósito, M. J. (2005). Influence of hormonal status on enkephalin-degrading aminopeptidase activity in the HPA axis of female mice. Gen. Comp. Endocrinol. 141, 135–140.
Influence of hormonal status on enkephalin-degrading aminopeptidase activity in the HPA axis of female mice.Crossref | GoogleScholarGoogle Scholar | 15748714PubMed |

Gentry, L. R., Thompson, D. L., Gentry, G. T., Davis, K. A., Godke, R. A., and Cartmill, J. A. (2002). The relationship between body condition, leptin and reproductive and hormonal characteristics of mares during the seasonal anovulatory period. J. Anim. Sci. 80, 2695–2703.
| 1:CAS:528:DC%2BD38XnvFGju7w%3D&md5=c9d374c438cf8e9fb626f7f1f8a2f885CAS | 12413093PubMed |

Heidler, B., Parvizi, N., Sauerwein, H., Bruckmaier, R. M., Heintges, U., Aurich, J. E., and Aurich, C. (2003). Effects of lactation on metabolic and reproductive hormones in Lipizzaner mares. Domest. Anim. Endocrinol. 25, 47–59.
Effects of lactation on metabolic and reproductive hormones in Lipizzaner mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVCiu7k%3D&md5=547632cf0cc817f9007c06f929d65392CAS | 12963098PubMed |

Hileman, S. M., Tornøe, J., Flier, J. S., and Bjørbaek, C. (2000). Transcellular transport of leptin by the short leptin receptor isoform ObRa in Madin–Darby canine kidney cells. Endocrinology 141, 1955–1961.
Transcellular transport of leptin by the short leptin receptor isoform ObRa in Madin–Darby canine kidney cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Wnu7w%3D&md5=14c4b323f5d06bd052455bf2c951d5c9CAS | 10830277PubMed |

Huff, N. K., Thompson, D. L.,, Gentry, L. R., and Depew, C. G. (2008). Hyperleptinemia in mares: prevalence in lactating mares and effect on rebreeding success. J. Equine Vet. Sci. 28, 579–586.
Hyperleptinemia in mares: prevalence in lactating mares and effect on rebreeding success.Crossref | GoogleScholarGoogle Scholar |

Kane, R. A., Fisher, M., Parrett, D., and Lawrence, L. M. (1987). Estimating fatness in horses. In ‘Proceedings of the 10th Equine Nutrition and Physiology Symposium, Fort Collins’. pp. 127–131. (Equine Nutrition and Physiology Society: Savoy, IL.)

Kawamura, K., Sato, N., Fukuda, J., Kodama, H., Kumagai, J., Tanikawa, H., Murata, M., and Tanaka, T. (2003). The role of leptin during the development of mouse preimplantation embryos. Mol. Cell. Endocrinol. 202, 185–189.
The role of leptin during the development of mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFSntrw%3D&md5=6ed3154f734994b12cb73013e3488464CAS | 12770749PubMed |

Kearns, C. F., McKeever, K. H., Roegner, V., Brady, S. M., and Malinowski, K. (2006). Adiponectin and leptin are related to fat mass in horses. Vet. J. 172, 460–465.
Adiponectin and leptin are related to fat mass in horses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSktLzE&md5=458ed06b8044ced4eaf831ffa4146ad6CAS | 15996495PubMed |

Kim, M. S., Yang, H. W., Kwon, H. C., Hwang, K. J., Kim, S. K., and Yoon, Y. D. (1999). Expression of leptin and its receptors in rat ovary. In ‘Society for the Study of Fertility, Annual Conference, Aberystwyth’. p. 108. (Journals of Reproduction and Fertility Ltd: Cambridge.)

Kim, H. S., Lee, G. S., Kim, J. H., Kang, S. K., Lee, B. C., and Hwang, W. S. (2006). Expression of leptin ligand and receptor and effect of exogenous leptin supplement on in vitro development of porcine embryos. Theriogenology 65, 831–844.
Expression of leptin ligand and receptor and effect of exogenous leptin supplement on in vitro development of porcine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCrsrY%3D&md5=7e72181e76e9dbdad03966ae866d393bCAS | 16356543PubMed |

Lange Consiglio, A., Dell’Aquila, M. E., Fiandanese, N., Ambruosi, B., Cho, Y. S., Bosi, G., Arrighi, S., Lacalandra, G. M., and Cremonesi, F. (2009). Effects of leptin on in vitro maturation, fertilization and embryonic cleavage after ICSI and early developmental expression of leptin (Ob) and leptin receptor (ObR) proteins in the horse. Reprod. Biol. Endocrinol. 7, 113.
Effects of leptin on in vitro maturation, fertilization and embryonic cleavage after ICSI and early developmental expression of leptin (Ob) and leptin receptor (ObR) proteins in the horse.Crossref | GoogleScholarGoogle Scholar | 19835605PubMed |

Maffei, M., Halaas, J., Ravussin, E., Pratley, R. E., Lee, G. H., Zhang, Y., Fei, H., Kim, S., Lallone, R., and Ranganathan, S. (1995). Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat. Med. 1, 1155–1161.
Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptFahs7s%3D&md5=8c8774abe46eb12ac12113082997c235CAS | 7584987PubMed |

Marchal, R., Vigneron, C., Perreau, C., Bali-Papp, A., and Mermillod, P. (2002). Effect of follicular size on meiotic and developmental competence of porcine oocytes. Theriogenology 57, 1523–1532.
Effect of follicular size on meiotic and developmental competence of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zhtFykug%3D%3D&md5=9ea42c649f9a05c3dce40a333be0bd2bCAS | 12054210PubMed |

McManus, C. J., and Fitzgerald, B. P. (2003). Effect of daily clenbuterol and exogenous melatonin treatment on body fat, serum leptin and the expression of seasonal anoestrus in the mare. Anim. Reprod. Sci. 76, 217–230.
Effect of daily clenbuterol and exogenous melatonin treatment on body fat, serum leptin and the expression of seasonal anoestrus in the mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVCgtLo%3D&md5=089c9aa362181e0da2545ca1b8ceda48CAS | 12586494PubMed |

Paula-Lopes, F. F., Boelhauve, M., Habermann, F. A., Sinowatz, F., and Wolf, E. (2007). Leptin promotes meiotic progression and developmental capacity of bovine oocytes via cumulus cell-independent and -dependent mechanisms. Biol. Reprod. 76, 532–541.
Leptin promotes meiotic progression and developmental capacity of bovine oocytes via cumulus cell-independent and -dependent mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlWhu7Y%3D&md5=3fa6992b28e6c33b7255ba75c8a43a1aCAS | 17093200PubMed |

Piccione, G., Bertolucci, C., Foà, A., and Caola, G. (2004). Influence of fasting and exercise on the daily rhythm of serum leptin in the horse. Chronobiol. Int. 21, 405–417.
Influence of fasting and exercise on the daily rhythm of serum leptin in the horse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFajsb8%3D&md5=0bb5e69b3837c29b409dd19583ef6b5fCAS | 15332446PubMed |

Pocar, P., Augustin, R., and Fischer, B. (2004). Constitutive expression of CYP1A1 in bovine cumulus–oocyte complexes in vitro: mechanisms and biological implications. Endocrinology 145, 1594–1601.
Constitutive expression of CYP1A1 in bovine cumulus–oocyte complexes in vitro: mechanisms and biological implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1Sjurc%3D&md5=e3f160cb5cbc61a69784c3d088584fdeCAS | 14726445PubMed |

Ruiz-Cortés, Z. T., Men, T., Palin, M. F., Downey, B. R., Lacroix, D. A., and Murphy, B. D. (2000). Porcine leptin receptor: molecular structure and expression in the ovary. Mol. Reprod. Dev. 56, 465–474.
Porcine leptin receptor: molecular structure and expression in the ovary.Crossref | GoogleScholarGoogle Scholar | 10911396PubMed |

Ryan, N. K., Van der Hoek, K. H., Robertson, S. A., and Norman, R. J. (2003). Leptin and leptin receptor expression in the rat ovary. Endocrinology 144, 5006–5013.
Leptin and leptin receptor expression in the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosleru7w%3D&md5=a53091b4c4e108c3ead8bd95bec78185CAS | 12959975PubMed |

Spicer, L. J. (2001). Leptin: a possible metabolic signal affecting reproduction. Domest. Anim. Endocrinol. 21, 251–270.
Leptin: a possible metabolic signal affecting reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFWgu7s%3D&md5=564f513797de2975f94d8ccbaf33c1c7CAS | 11872320PubMed |

Sun, Q. Y., Lai, L., Bonk, A., Prather, R. S., and Schatten, H. (2001). Cytoplasmic changes in relation to nuclear maturation and early embryo developmental potential of porcine oocytes: effects of gonadotrophins, cumulus cells, follicular size and protein synthesis inhibition. Mol. Reprod. Dev. 59, 192–198.
Cytoplasmic changes in relation to nuclear maturation and early embryo developmental potential of porcine oocytes: effects of gonadotrophins, cumulus cells, follicular size and protein synthesis inhibition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsVals7k%3D&md5=7352d3b43a9afa59124b87b10632c0e9CAS | 11389554PubMed |

Tartaglia, L. A., Dembski, M., Weng, X., Deng, N., Culpepper, J., Devos, R., Richards, G. J., Campfield, L. A., Clark, F. T., Deeds, J., Muir, C., Sanker, S., Moriarty, A., Moore, K. J., Smutko, J. S., Mays, G. G., Wool, E. A., Monroe, C. A., and Tepper, R. I. (1995). Identification and expression cloning of a leptin receptor, OB-R. Cell 83, 1263–1271.
Identification and expression cloning of a leptin receptor, OB-R.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhsVOmtg%3D%3D&md5=7c8b529e1862a71ad44664afdf19ca94CAS | 8548812PubMed |

Uotani, S., Bjørbaek, C., Tornøe, J., and Flier, J. S. (1999). Functional properties of leptin receptor isoforms: internalization and degradation of leptin and ligand-induced receptor downregulation. Diabetes 48, 279–286.
Functional properties of leptin receptor isoforms: internalization and degradation of leptin and ligand-induced receptor downregulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpsFKntg%3D%3D&md5=5d846db208d1150c5c0c09962928a107CAS | 10334302PubMed |

Waller, C. A., Thompson, D. L., Cartmill, J. A., Storer, W. A., and Huff, N. K. (2006). Reproduction in high-body-condition mares with high versus low leptin concentrations. Theriogenology 66, 923–928.
Reproduction in high-body-condition mares with high versus low leptin concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1Wrtbk%3D&md5=6827effdccf82a1cdc3b5c55783f30d1CAS | 16566994PubMed |

Wunder, D. M., Mueller, M. D., Birkhäuser, M. H., and Bersinger, N. A. (2005). Steroids and protein markers in the follicular fluid as indicators of oocyte quality in patients with and without endometriosis. J. Assist. Reprod. Genet. 22, 257–264.
Steroids and protein markers in the follicular fluid as indicators of oocyte quality in patients with and without endometriosis.Crossref | GoogleScholarGoogle Scholar | 16021855PubMed |

Yoon, K. W., Shin, T. Y., Park, J. I., Roh, S., Lim, J. M., Lee, B. C., Hwang, W. S., and Lee, E. S. (2000). Development of porcine oocytes from preovulatory follicles of different sizes after maturation in media supplemented with follicular fluids. Reprod. Fertil. Dev. 12, 133–139.
Development of porcine oocytes from preovulatory follicles of different sizes after maturation in media supplemented with follicular fluids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvjsFejtw%3D%3D&md5=ef6fb2fb231501259596cf6fe192cd59CAS | 11302422PubMed |

Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., and Friedman, J. M. (1994). Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425–432.
Positional cloning of the mouse obese gene and its human homologue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisVGqsbs%3D&md5=8b8830065b202eb56e701597fd5ea0ddCAS | 7984236PubMed |