β-nerve growth factor identification in male rabbit genital tract and seminal plasma and its role in ovulation induction in rabbit does

Abstract The neurotrophin β-nerve growth factor (NGF) has been described as an important mediator of seminal plasma-induced ovulation in reflexive ovulators like camelids, but this action has not been evidenced in rabbits. In this study, the mRNA expression of NGF was analysed in rabbit male organs by PCR and in a purified basic fraction of seminal plasma by liquid chromatography mass spectrometry. Besides, the ovulatory response [ovulation rate (OR), corpora lutea number, LH peak and progesterone profile] of 27 rabbit does was recorded after injection with murine NGF, gonadoreline (GnRH) or saline solution (SS). An empty catheter was introduced through the vagina (n = 4 animals per group) to simulate the nervous/mechanical stimulus of coitus. Molecular studies confirmed the expression of β-NGF mRNA in the prostate, seminal gland and testicles of male adult rabbits, and the presence of the protein in seminal plasma. For the in vivo experiment, all GnRH-group does exhibited a significantly higher OR (100%) compared to females treated with NGF (30%) and SS (25%), who showed significantly lower LH and progesterone concentrations at 120 min. However, in the non-vaginally stimulated animals, only the gonadoreline group ovulated properly, since no ovulation was recorded in the SS group, and only 17% of the NGF does ovulated; this was associated to a tendency to a higher rate of anovulatory haemorrhagic follicles. mRNA expression of NGF and its presence in seminal plasma evidence a role in rabbit reproduction. Nevertheless, murine NGF triggered some stimulatory effect in the females but not enough to elicit a significant ovulatory response.

[1]  Melissa R. Pergande,et al.  Isoelectric Point Separations of Peptides and Proteins , 2017, Proteomes.

[2]  G. Adams,et al.  Ovulation-inducing factor (OIF/NGF) in seminal plasma: a review and update. , 2016, Reproduction in domestic animals = Zuchthygiene.

[3]  M. Maranesi,et al.  Expression of nerve growth factor and its receptors in the uterus of rabbits: functional involvement in prostaglandin synthesis. , 2016, Domestic animal endocrinology.

[4]  M. Viudes-de-Castro,et al.  Can the Genetic Origin Affect Rabbit Seminal Plasma Protein Profile along the Year? , 2016, Reproduction in domestic animals = Zuchthygiene.

[5]  M. Maranesi,et al.  Gene Expression and Localization of NGF and Its Cognate Receptors NTRK1 and NGFR in the Sex Organs of Male Rabbits. , 2015, Reproduction in domestic animals = Zuchthygiene.

[6]  S. D. de Graaf,et al.  Effects of varying doses of β-nerve growth factor on the timing of ovulation, plasma progesterone concentration and corpus luteum size in female alpacas (Vicugna pacos). , 2015, Reproduction, fertility, and development.

[7]  G. Adams,et al.  LH release and ovulatory response after intramuscular, intravenous, and intrauterine administration of β-nerve growth factor of seminal plasma origin in female llamas. , 2015, Theriogenology.

[8]  G. Adams,et al.  Bioactivity of ovulation inducing factor (or nerve growth factor) in bovine seminal plasma and its effects on ovarian function in cattle. , 2015, Theriogenology.

[9]  C. Castellini,et al.  271 INDUCTION OF OVULATION IN RABBIT DOES USING PURIFIED NERVE GROWTH FACTOR AND CAMEL SEMINAL PLASMA , 2015 .

[10]  G. Adams,et al.  In vivo imaging in the rabbit as a model for the study of ovulation-inducing factors , 2015, Laboratory animals.

[11]  G. Adams,et al.  Ovulation-inducing factor (OIF/NGF) from seminal plasma origin enhances Corpus Luteum function in llamas regardless the preovulatory follicle diameter. , 2014, Animal reproduction science.

[12]  M. Maranesi,et al.  Expression of the cannabinoid receptor type 1 in the pituitary of rabbits and its role in the control of LH secretion. , 2013, Domestic animal endocrinology.

[13]  B. Crossett,et al.  Proteomic characterization and cross species comparison of mammalian seminal plasma. , 2013, Journal of proteomics.

[14]  G. Mal,et al.  Proteomic identification of camel seminal plasma: purification of β-nerve growth factor. , 2013, Animal reproduction science.

[15]  G. Adams,et al.  Ovulation-inducing factor in seminal plasma: a review. , 2013, Animal reproduction science.

[16]  J. Vaughan,et al.  β-Nerve growth factor is a major component of alpaca seminal plasma and induces ovulation in female alpacas. , 2012, Reproduction, fertility, and development.

[17]  G. Adams,et al.  Effect of purified llama ovulation-inducing factor (OIF) on ovarian function in cattle. , 2012, Theriogenology.

[18]  L. Delbaere,et al.  The nerve of ovulation-inducing factor in semen , 2012, Proceedings of the National Academy of Sciences.

[19]  G. Adams,et al.  Ovarian estradiol modulates the stimulatory effect of ovulation-inducing factor (OIF) on pituitary LH secretion in llamas. , 2012, Theriogenology.

[20]  L. Sylla,et al.  Ovulating induction methods in rabbit does: the pituitary and ovarian responses. , 2012, Theriogenology.

[21]  G. Adams,et al.  Is an ovulation-inducing factor (OIF) present in the seminal plasma of rabbits? , 2011, Animal reproduction science.

[22]  G. Adams,et al.  Dose-Response of Female Llamas to Ovulation-Inducing Factor from Seminal Plasma1 , 2011, Biology of reproduction.

[23]  G. Adams,et al.  Evidence for the conservation of biological activity of ovulation-inducing factor in seminal plasma. , 2011, Reproduction.

[24]  H. Rodríguez-Martínez,et al.  Seminal Plasma Proteins: What Role Do They Play? , 2011, American journal of reproductive immunology.

[25]  Chunjin Li,et al.  Detection of nerve growth factor (NGF) and its specific receptor (TrkA) in ejaculated bovine sperm, and the effects of NGF on sperm function. , 2010, Theriogenology.

[26]  Chunjin Li,et al.  Absence of nerve growth factor and comparison of tyrosine kinase receptor A levels in mature spermatozoa from oligoasthenozoospermic, asthenozoospermic and fertile men. , 2010, Clinica chimica acta; international journal of clinical chemistry.

[27]  M. Maranesi,et al.  Expression of luteal estrogen receptor, interleukin-1, and apoptosis-associated genes after PGF2alpha administration in rabbits at different stages of pseudopregnancy. , 2010, Domestic animal endocrinology.

[28]  H. Matsuda,et al.  Effect of NGF on the motility and acrosome reaction of golden hamster spermatozoa in vitro. , 2010, The Journal of reproduction and development.

[29]  G. Adams,et al.  Comparison of the effect of ovulation-inducing factor (OIF) in the seminal plasma of llamas, alpacas, and bulls. , 2006, Theriogenology.

[30]  D. Svergun,et al.  Structural and functional properties of mouse proNGF. , 2006, Biochemical Society transactions.

[31]  G. Adams,et al.  Ovulation-Inducing Factor in the Seminal Plasma of Alpacas and Llamas1 , 2005, Biology of reproduction.

[32]  K. Unsicker,et al.  The seminal vesicle of the bull: a new and very rich source of nerve growth factor. , 2005, European journal of biochemistry.

[33]  T. Bączek.  Fractionation of peptides in proteomics with the use of pI-based approach and ZipTip pipette tips. , 2004, Journal of pharmaceutical and biomedical analysis.

[34]  Salvatore Sechi,et al.  A method to identify and simultaneously determine the relative quantities of proteins isolated by gel electrophoresis. , 2002, Rapid communications in mass spectrometry : RCM.

[35]  B. Hempstead.  The many faces of p75NTR , 2002, Current Opinion in Neurobiology.

[36]  D. Li,et al.  Isolation and purification of the ovulation-inducing factor from seminal plasma in the bactrian camel (Camelus bactrianus). , 2001, Theriogenology.

[37]  S. Ojeda,et al.  Neurotrophic and cell–cell dependent control of early follicular development , 2000, Molecular and Cellular Endocrinology.

[38]  G. Adler,et al.  Commercial Recombinant Human β‐Nerve Growth Factor and Adult Rat Dorsal Root Ganglia Contain an Identical Molecular Species of Nerve Growth Factor Prohormone , 2000, Journal of neurochemistry.

[39]  R. Middendorff,et al.  Neurotrophic factors in the testis , 1999 .

[40]  L. Campagnolo,et al.  Spatiotemporal patterns of expression of neurotrophins and neurotrophin receptors in mice suggest functional roles in testicular and epididymal morphogenesis. , 1999, Biology of reproduction.

[41]  J. Alvariño,et al.  Effect of gonadoreline and naloxone on induction of ovulation and plasma LH in rabbit. , 1997, Revista espanola de fisiologia.

[42]  S. Ojeda,et al.  Participation of nerve growth factor in the regulation of ovarian function , 1996, Zygote.

[43]  P. Rebollar,et al.  Influence of the postpartum day on plasma estradiol-17 β levels, sexual behaviour, and conception rate, in artificially inseminated lactating rabbits , 1995 .

[44]  Y. Barde,et al.  Characterisation of neurotrophin dimers and monomers. , 1994, European journal of biochemistry.

[45]  R. Legro,et al.  Pregnancy: Premature luteinization as detected by elevated serum progesterone is associated with a higher pregnancy rate in donor oocyte in-vitro fertilization , 1993 .

[46]  J. Toppari,et al.  Expression of beta-nerve growth factor and its receptor in rat seminiferous epithelium: specific function at the onset of meiosis , 1992, The Journal of cell biology.

[47]  T. Hökfelt,et al.  Expression of beta-nerve growth factor receptor mRNA in Sertoli cells downregulated by testosterone. , 1990, Science.

[48]  T. Meyer,et al.  Nerve growth factor (NGF) is present in human placenta and semen, but undetectable in normal and Paget's disease blood: measurements with an anti-mouse-NGF enzyme immunoassay using a recombinant human NGF reference. , 1988, Biochemical and biophysical research communications.

[49]  Y. Gao,et al.  Hormone concentrations before and after semen-induced ovulation in the bactrian camel (Camelus bactrianus). , 1985, Journal of reproduction and fertility.

[50]  G. Pan,et al.  Semen-induced ovulation in the bactrian camel (Camelus bactrianus). , 1985, Journal of reproduction and fertility.

[51]  J. Miller,et al.  Characterization and physiological variation of estrogen receptors in rabbit corpora lutea throughout pregnancy and pseudopregnancy: the effect of hysterectomy and sustained estradiol treatment. , 1983, Biology of reproduction.

[52]  H. Thoenen,et al.  The purification of nerve growth factor from bovine seminal plasma. Biochemical characterization and partial amino acid sequence. , 1982, The Journal of biological chemistry.

[53]  H. Thoenen,et al.  The Distribution of Nerve Growth Factor in the Male Sex Organs of Mammals , 1980, Journal of neurochemistry.

[54]  G. Burnstock,et al.  Guinea pig prostate is a rich source of nerve growth factor , 1979, Nature.

[55]  P. Franchimont,et al.  Time-courses of LH and FSH release after mating in the female rabbit. , 1973, Endocrinology.

[56]  R. E. Staples.  Behavioural induction of ovulation in the oestrous rabbit. , 1967, Journal of reproduction and fertility.

[57]  C. Sawyer,et al.  Estrogen facilitation of release of pituitary ovulating hormone in the rabbit in response to vaginal stimulation. , 1959, Endocrinology.

[58]  M. Masdeu,et al.  188 EFFECT OF RABBIT SEMINAL PLASMA IN OVULATING RESPONSE , 2013 .

[59]  G. Evans,et al.  Seminal plasma effects on sperm handling and female fertility. , 2007, Society of Reproduction and Fertility supplement.

[60]  G. Adams,et al.  Reproductive Biology and Endocrinology Open Access Local versus Systemic Effect of Ovulation-inducing Factor in the Seminal Plasma of Alpacas , 2005 .

[61]  C. Erck,et al.  Expression of nerve growth factor and neurotrophin receptors in testicular cells suggest novel roles for neurotrophins outside the nervous system. , 1996, Reproduction, fertility, and development.