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Kisspeptin signaling is required for the luteinizing hormone response in anestrous ewes following the introduction of males.

De Bond JA, Li Q, Millar RP, Clarke IJ, Smith JT - PLoS ONE (2013)

Bottom Line: Introduction of a male led to elevated mean LH levels, due to increased LH pulse amplitude and pulse frequency in females, when compared to females not exposed to a male.Brains were collected after the male effect stimulus and we observed an increase in the percentage of kisspeptin neurons co-expressing Fos, by immunohistochemistry.We conclude that introduction of male sheep to seasonally anestrous female sheep activates kisspeptin neurons and other cells in the hypothalamus, leading to increased GnRH/LH secretion.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Monash University, Melbourne, Victoria, Australia.

ABSTRACT
The introduction of a novel male stimulates the hypothalamic-pituitary-gonadal axis of female sheep during seasonal anestrus, leading to the resumption of follicle maturation and ovulation. How this pheromone cue activates pulsatile secretion of gonadotropin releasing hormone (GnRH)/luteinizing hormone (LH) is unknown. We hypothesised that pheromones activate kisspeptin neurons, the product of which is critical for the stimulation of GnRH neurons and fertility. During the non-breeding season, female sheep were exposed to novel males and blood samples collected for analysis of plasma LH profiles. Females without exposure to males served as controls. In addition, one hour before male exposure, a kisspeptin antagonist (P-271) or vehicle was infused into the lateral ventricle and continued for the entire period of male exposure. Introduction of a male led to elevated mean LH levels, due to increased LH pulse amplitude and pulse frequency in females, when compared to females not exposed to a male. Infusion of P-271 abolished this effect of male exposure. Brains were collected after the male effect stimulus and we observed an increase in the percentage of kisspeptin neurons co-expressing Fos, by immunohistochemistry. In addition, the per-cell expression of Kiss1 mRNA was increased in the rostral and mid (but not the caudal) arcuate nucleus (ARC) after male exposure in both aCSF and P-271 treated ewes, but the per-cell content of neurokinin B mRNA was decreased. There was also a generalized increase in Fos positive cells in the rostral and mid ARC as well as the ventromedial hypothalamus of females exposed to males. We conclude that introduction of male sheep to seasonally anestrous female sheep activates kisspeptin neurons and other cells in the hypothalamus, leading to increased GnRH/LH secretion.

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Male exposure in anestrous ewes resulted in Fos induction in ARC kisspeptin neurons.A, Bright-field photomicrographs indicate kisspeptin (brown) and Fos (black) neurons (arrows) in the rostral ARC. Scale bar, 50 µm. B–D, In the rostral (B) and mid (C) ARC, the percentage of kisspeptin cells co-expressing Fos was greater in male exposed ewes (note: kisspeptin antagonist treatment did not alter Fos induction in kisspeptin cells). No change was evident in the caudal ARC (D). E-G, The number of kisspeptin/Fos neurons was also higher in male exposed ewes in the rostral (E) and mid (F) ARC. Data are the mean ± SEM, *P<0.05, n = 4 per group.
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pone-0057972-g003: Male exposure in anestrous ewes resulted in Fos induction in ARC kisspeptin neurons.A, Bright-field photomicrographs indicate kisspeptin (brown) and Fos (black) neurons (arrows) in the rostral ARC. Scale bar, 50 µm. B–D, In the rostral (B) and mid (C) ARC, the percentage of kisspeptin cells co-expressing Fos was greater in male exposed ewes (note: kisspeptin antagonist treatment did not alter Fos induction in kisspeptin cells). No change was evident in the caudal ARC (D). E-G, The number of kisspeptin/Fos neurons was also higher in male exposed ewes in the rostral (E) and mid (F) ARC. Data are the mean ± SEM, *P<0.05, n = 4 per group.

Mentions: Kisspeptin cells co-expressing Fos were readily detected in the ARC of ewes (Figure 3A). In the rostral ARC, male exposure in anestrous ewes resulted in a 9-fold increase in the percentage of kisspeptin cells co-labeling for Fos compared with controls (P<0.001, Figure 3B). Infusion of P-271 did not prevent the increase in kisspeptin neuron activation following male exposure. Similar results were seen in the mid ARC (3-fold increase in male-exposed ewes, P<0.05, Figure 3C) and there was no change in the caudal ARC (Figure 3D). The number of kisspeptin/Fos neurons also increased following male exposure in the rostral (P<0.01, Figure 3E) and mid (P<0.05, Figure 3F) ARC and infusion of P-271 did not prevent this increase. No change was again noted in the caudal ARC (Figure 3G).


Kisspeptin signaling is required for the luteinizing hormone response in anestrous ewes following the introduction of males.

De Bond JA, Li Q, Millar RP, Clarke IJ, Smith JT - PLoS ONE (2013)

Male exposure in anestrous ewes resulted in Fos induction in ARC kisspeptin neurons.A, Bright-field photomicrographs indicate kisspeptin (brown) and Fos (black) neurons (arrows) in the rostral ARC. Scale bar, 50 µm. B–D, In the rostral (B) and mid (C) ARC, the percentage of kisspeptin cells co-expressing Fos was greater in male exposed ewes (note: kisspeptin antagonist treatment did not alter Fos induction in kisspeptin cells). No change was evident in the caudal ARC (D). E-G, The number of kisspeptin/Fos neurons was also higher in male exposed ewes in the rostral (E) and mid (F) ARC. Data are the mean ± SEM, *P<0.05, n = 4 per group.
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Related In: Results  -  Collection

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pone-0057972-g003: Male exposure in anestrous ewes resulted in Fos induction in ARC kisspeptin neurons.A, Bright-field photomicrographs indicate kisspeptin (brown) and Fos (black) neurons (arrows) in the rostral ARC. Scale bar, 50 µm. B–D, In the rostral (B) and mid (C) ARC, the percentage of kisspeptin cells co-expressing Fos was greater in male exposed ewes (note: kisspeptin antagonist treatment did not alter Fos induction in kisspeptin cells). No change was evident in the caudal ARC (D). E-G, The number of kisspeptin/Fos neurons was also higher in male exposed ewes in the rostral (E) and mid (F) ARC. Data are the mean ± SEM, *P<0.05, n = 4 per group.
Mentions: Kisspeptin cells co-expressing Fos were readily detected in the ARC of ewes (Figure 3A). In the rostral ARC, male exposure in anestrous ewes resulted in a 9-fold increase in the percentage of kisspeptin cells co-labeling for Fos compared with controls (P<0.001, Figure 3B). Infusion of P-271 did not prevent the increase in kisspeptin neuron activation following male exposure. Similar results were seen in the mid ARC (3-fold increase in male-exposed ewes, P<0.05, Figure 3C) and there was no change in the caudal ARC (Figure 3D). The number of kisspeptin/Fos neurons also increased following male exposure in the rostral (P<0.01, Figure 3E) and mid (P<0.05, Figure 3F) ARC and infusion of P-271 did not prevent this increase. No change was again noted in the caudal ARC (Figure 3G).

Bottom Line: Introduction of a male led to elevated mean LH levels, due to increased LH pulse amplitude and pulse frequency in females, when compared to females not exposed to a male.Brains were collected after the male effect stimulus and we observed an increase in the percentage of kisspeptin neurons co-expressing Fos, by immunohistochemistry.We conclude that introduction of male sheep to seasonally anestrous female sheep activates kisspeptin neurons and other cells in the hypothalamus, leading to increased GnRH/LH secretion.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Monash University, Melbourne, Victoria, Australia.

ABSTRACT
The introduction of a novel male stimulates the hypothalamic-pituitary-gonadal axis of female sheep during seasonal anestrus, leading to the resumption of follicle maturation and ovulation. How this pheromone cue activates pulsatile secretion of gonadotropin releasing hormone (GnRH)/luteinizing hormone (LH) is unknown. We hypothesised that pheromones activate kisspeptin neurons, the product of which is critical for the stimulation of GnRH neurons and fertility. During the non-breeding season, female sheep were exposed to novel males and blood samples collected for analysis of plasma LH profiles. Females without exposure to males served as controls. In addition, one hour before male exposure, a kisspeptin antagonist (P-271) or vehicle was infused into the lateral ventricle and continued for the entire period of male exposure. Introduction of a male led to elevated mean LH levels, due to increased LH pulse amplitude and pulse frequency in females, when compared to females not exposed to a male. Infusion of P-271 abolished this effect of male exposure. Brains were collected after the male effect stimulus and we observed an increase in the percentage of kisspeptin neurons co-expressing Fos, by immunohistochemistry. In addition, the per-cell expression of Kiss1 mRNA was increased in the rostral and mid (but not the caudal) arcuate nucleus (ARC) after male exposure in both aCSF and P-271 treated ewes, but the per-cell content of neurokinin B mRNA was decreased. There was also a generalized increase in Fos positive cells in the rostral and mid ARC as well as the ventromedial hypothalamus of females exposed to males. We conclude that introduction of male sheep to seasonally anestrous female sheep activates kisspeptin neurons and other cells in the hypothalamus, leading to increased GnRH/LH secretion.

Show MeSH
Related in: MedlinePlus