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Vertebrate reproductive science and technology
RESEARCH ARTICLE

β-Nerve growth factor is a major component of alpaca seminal plasma and induces ovulation in female alpacas

C. M. Kershaw-Young A D , X. Druart B , J. Vaughan C and W. M. C. Maxwell A
+ Author Affiliations
- Author Affiliations

A Faculty of Veterinary Science, The University of Sydney, Camperdown, NSW 2006, Australia.

B UMR 6175, Inra-Cnrs-Université de Tours-Haras Nationaux, 37380, Nouzilly, France.

C Cria Genesis, PO Box 406, Ocean Grove, Vic. 3226, Australia.

D Corresponding author. Email: claire.kershawyoung@yahoo.co.uk

Reproduction, Fertility and Development 24(8) 1093-1097 https://doi.org/10.1071/RD12039
Submitted: 14 February 2012  Accepted: 10 March 2012   Published: 24 April 2012

Abstract

Ovulation in camelids is induced by an unidentified protein in the seminal plasma of the male termed ‘ovulation-inducing factor’. This protein has been reported to be a 14-kDa protein under reducing conditions, which, when purified from seminal plasma, induces ovulation in llamas. The identification of this protein and investigation of its potential to induce ovulation in camelids may aid the development of protocols for the induction of ovulation. In the present study, alpaca seminal plasma proteins were separated using one-dimensional sodium dodecyl sulfate–polyacrylamide gel electrophoresis and the most abundant protein of 14 kDa was identified as β-nerve growth factor (β-NGF) by liquid chromatography mass spectrometry. Female alpacas (n = 5 per group) were given intramuscular injections of: (1) 1 mL of 0.9% saline; (2) 4 µg buserelin, a gonadotrophin-releasing hormone agonist; (3) 2 mL alpaca seminal plasma; or (4) 1 mg human β-NGF. Ovulation was detected by transrectal ultrasonography 8 days after treatment and confirmed by plasma progesterone concentrations. Ovulation occurred in 0%, 80%, 80% and 80% of animals treated with saline, buserelin, seminal plasma and β-NGF, respectively. Treatment type did not affect the diameter of the corpus luteum, but plasma progesterone concentrations were lower in saline-treated animals than in the other treatment groups owing to the lack of a corpus luteum. The present study is the first to identify the ovulation-inducing factor protein in alpacas. β-NGF successfully induces ovulation in alpacas and this finding may lead to new methods for the induction of ovulation in camelids.

Additional keywords: camelid, ovulation inducing factor.


References

Adams, G. P., Ratto, M. H., Huanca, W., and Singh, J. (2005). Ovulation-inducing factor in the seminal plasma of alpacas and llamas. Biol. Reprod. 73, 452–457.
Ovulation-inducing factor in the seminal plasma of alpacas and llamas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovV2qt7s%3D&md5=3754e66b0a65d67776fff60216881de0CAS | 15888733PubMed |

Bogle, O. A., Ratto, M. H., and Adams, G. P. (2011). Evidence for the conservation of biological activity of ovulation-inducing factor in seminal plasma. Reproduction 142, 277–283.
Evidence for the conservation of biological activity of ovulation-inducing factor in seminal plasma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2gs73M&md5=7a2f45901f9bf94cc384fc732e9ebc93CAS | 21652637PubMed |

Bravo, P. W., Flores, U., Garnica, J., and Ordonez, C. (1997). Collection of semen and artificial insemination of alpacas. Theriogenology 47, 619–626.
Collection of semen and artificial insemination of alpacas.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVOltQ%3D%3D&md5=637b950f022d51f63fd7807de7706e66CAS | 16728014PubMed |

Bravo, P. W., Skidmore, J. A., and Zhao, X. X. (2000). Reproductive aspects and storage of semen in camelidae. Anim. Reprod. Sci. 62, 173–193.
Reproductive aspects and storage of semen in camelidae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Kgtr4%3D&md5=804ec852feee0e76eea74e5c4bcb5ec8CAS | 10924824PubMed |

Chen, B. X., Yuen, Z. X., and Pan, G. W. (1985). Semen-induced ovulation in the bactrian camel (Camelus bactrianus). J. Reprod. Fertil. 74, 335–339.
Semen-induced ovulation in the bactrian camel (Camelus bactrianus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2FhtFWhug%3D%3D&md5=ebac602fd6b4f4af57d6958ce24e8602CAS | 3900379PubMed |

Dissen, G. A., Hill, D. F., Costa, M. E., Dees, W. L., Lara, H. E., and Ojeda, S. R. (1996a). A role for trka nerve growth factor receptors in mammalian ovulation. Endocrinology 137, 198–209.
A role for trka nerve growth factor receptors in mammalian ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhsVOrsA%3D%3D&md5=53d32d8c57f545720bd9bee7fcaa9ad2CAS | 8536613PubMed |

Dissen, G. A., Mayerhofer, A., and Ojeda, S. R. (1996b). Participation of nerve growth factor in the regulation of ovarian function. Zygote 4, 309–312.
Participation of nerve growth factor in the regulation of ovarian function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsFalsb8%3D&md5=36e00eb6d0449937e35b626fadf6b7d0CAS | 9153771PubMed |

Garnica, J., Achata, R., and Bravo, P. W. (1993). Physical and biochemical characteristics of alpaca semen. Anim. Reprod. Sci. 32, 85–90.
Physical and biochemical characteristics of alpaca semen.Crossref | GoogleScholarGoogle Scholar |

Harper, G. P., and Theonen, H. (1980). The distribution of nerve growth factor in the male sex organs of mammals. J. Neurochem. 34, 893–903.
The distribution of nerve growth factor in the male sex organs of mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhslOqt7k%3D&md5=718296aeae3f2fe049e47ca6c0467515CAS | 6766987PubMed |

Harper, G. P., Barde, Y. A., Burnstock, G., Carstairs, J. R., Dennison, M. E., Suda, K., and Vernon, C. A. (1979). Guinea pig prostate is a rich source of nerve growth factor. Nature 279, 160–162.
Guinea pig prostate is a rich source of nerve growth factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlslahsb4%3D&md5=e5888c500364e458505d100ef26304e4CAS | 440421PubMed |

Harper, G. P., Glanville, R. W., and Thoenen, H. (1982). The purification of nerve growth factor from bovine seminal plasma. Biochemical characterization and partial amino acid sequence. J. Biol. Chem. 257, 8541–8542.
| 1:CAS:528:DyaL38XkvVGnt74%3D&md5=0320fa7c97d9933eef26d21d26dd7cb9CAS | 7085682PubMed |

Lichtenwalner, A. B., Woods, G. L., and Weber, J. A. (1996). Seminal collection, seminal charateristics and pattern of ejaculation in llamas. Theriogenology 46, 293–305.
Seminal collection, seminal charateristics and pattern of ejaculation in llamas.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVKmtw%3D%3D&md5=7bd794c1d1cc504dc86e1ea34b926d67CAS | 16727899PubMed |

MacGrogan, D., Despres, G., Romand, R., and Dicou, E. (1991). Expression of the β-nerve growth factor gene in male sex organs of the mouse, rat, and guinea pig. J. Neurosci. Res. 28, 567–573.
Expression of the β-nerve growth factor gene in male sex organs of the mouse, rat, and guinea pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXisVWgt74%3D&md5=6adc8732c8f668efde8d05266a9bb558CAS | 1714511PubMed |

Morton, K. M., Gibb, Z., Bertoldo, M., and Maxwell, W. M. C. (2009). Effect of diluent, dilution rate and storage temperature on longevity and functional integrity of liquid stored alpaca (Vicugna pacos) semen. J. Camelid Sci. 2, 15–25.

Pan, G., Chen, Z., Liu, X., Li, D., Xie, Q., Ling, F., and Fang, L. (2001). Isolation and purification of the ovulation-inducing factor from seminal plasma in the bactrian camel (Camelus bactrianus). Theriogenology 55, 1863–1879.
Isolation and purification of the ovulation-inducing factor from seminal plasma in the bactrian camel (Camelus bactrianus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvFarsbs%3D&md5=87203e1f7d9c81e3330575546077e7b0CAS | 11414491PubMed |

Paolicchi, F., Urquieta, B., Del Valle, L., and Bustos-Obregon, E. (1999). Biological activity of the seminal plasma of alpacas: stimulus for the production of LH by pituitary cells. Anim. Reprod. Sci. 54, 203–210.
Biological activity of the seminal plasma of alpacas: stimulus for the production of LH by pituitary cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXks1WqsA%3D%3D&md5=5bd93b6ce128bb511477cf9e89caa03cCAS | 10066107PubMed |

Ratto, M. H., Huanca, W., Singh, J., and Adams, G. P. (2005). Local versus systemic effect of ovulation-inducing factor in the seminal plasma of alpacas. Reprod. Biol. Endocrinol. 3, 29.
Local versus systemic effect of ovulation-inducing factor in the seminal plasma of alpacas.Crossref | GoogleScholarGoogle Scholar | 16018817PubMed |

Ratto, M. H., Huanca, W., Singh, J., and Adams, G. P. (2006). Comparison of the effect of ovulation-inducing factor (OIF) in the seminal plasma of llamas, alpacas, and bulls. Theriogenology 66, 1102–1106.
Comparison of the effect of ovulation-inducing factor (OIF) in the seminal plasma of llamas, alpacas, and bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotleqsLg%3D&md5=7fa29df64a5733e503027d65b0cfecb6CAS | 16630652PubMed |

Ratto, M. H., Huanca, W., and Adams, G. P. (2010). Ovulation-inducing factor: a protein component of llama seminal plasma. Reprod. Biol. Endocrinol. 8, 44–50.
Ovulation-inducing factor: a protein component of llama seminal plasma.Crossref | GoogleScholarGoogle Scholar | 20462434PubMed |

Ratto, M. H., Delbaere, L. T. J., Leduc, Y. A., Pierson, R. A., and Adams, G. P. (2011). Biochemical isolation and purification of ovulation-inducing factor (OIF) in seminal plasma of llamas. Reprod. Biol. Endocrinol. 9, 24–31.
Biochemical isolation and purification of ovulation-inducing factor (OIF) in seminal plasma of llamas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXivVegt7o%3D&md5=bf5d3e61a6e1f6d7ba92e62b2fa586c2CAS | 21310078PubMed |

Salas, C., Julio-Pieper, M., Valladares, M., Pommer, R., Vega, M., Mastronardi, C., Kerr, B., Ojeda, S. R., Lara, H. E., and Romero, C. (2006). Nerve growth factor-dependent activation of trka receptors in the human ovary results in synthesis of follicle-stimulating hormone receptors and estrogen secretion. J. Clin. Endocrinol. Metab. 91, 2396–2403.
Nerve growth factor-dependent activation of trka receptors in the human ovary results in synthesis of follicle-stimulating hormone receptors and estrogen secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVCgt7k%3D&md5=647b572cb6f4ab73f4cc0a93eac734c1CAS | 16537688PubMed |

Silva, M., Nino, A., Guerra, M., Letelier, C., Valderrama, X. P., Adams, G. P., and Ratto, M. H. (2011). Is an ovulation-inducing factor (OIF) present in the seminal plasma of rabbits? Anim. Reprod. Sci. 127, 213–221.
Is an ovulation-inducing factor (OIF) present in the seminal plasma of rabbits?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlChs7fK&md5=996f9b733721c98903ea9e1944ec4cb8CAS | 21899964PubMed |

Skidmore, J. A. (2011). Reproductive physiology in female Old World camelids. Anim. Reprod. Sci. 124, 148–154.
Reproductive physiology in female Old World camelids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlvFWhtLY%3D&md5=9704cff0cedf70a39eda17c2822181d9CAS | 20888154PubMed |

Sumar, J., Fredriksson, G., Alarcon, V., Kindahl, H., and Edqvist, L. (1988). Levels of 15-keto-13,14-dihydro-pgf2a, progesterone and estradiol-17-beta after induced ovulations in llamas and alpacas. Acta Vet. Scand. 29, 339–346.
| 1:CAS:528:DyaL1MXlt1Ohs7g%3D&md5=66f89c61837d049ce76eeec157c49bb4CAS | 3256233PubMed |

Tanco, V. M., Ratto, M. H., Lazzarotta, M., and Adams, G. P. (2011). Dose–response of female llamas to ovulation-inducing factor from seminal plasma. Biol. Reprod. 85, 452–456.
Dose–response of female llamas to ovulation-inducing factor from seminal plasma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2gtL3K&md5=fcd28c9e11fddc84a9f4197a110b7af1CAS | 21593475PubMed |

Tibary, J., and Vaughan, J. (2006). Reproductive infertility and physiology in male South American camelids: a review and clinical observations. Small Rumin. Res. 61, 283–298.
Reproductive infertility and physiology in male South American camelids: a review and clinical observations.Crossref | GoogleScholarGoogle Scholar |

Vaughan, J., Galloway, D., and Hopkins, D. (2003). ‘Artificial Insemination in Alpacas (Lama pacos).’ (Rural Industries Research and Development Corporation: Kingston, ACT.)

Wang, H., Dong, Y., Chen, W., Hei, J., and Dong, C. (2011). Expression and localization of nerve growth factor (NGF) in the testis of alpaca (Llama pacos). Folia Histochem. Cytobiol. 49, 55–61.
| 1:CAS:528:DC%2BC3MXhtVOntLvJ&md5=36418737ae5d7981691e2c8f93ed435eCAS | 21526490PubMed |