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. 2024 Aug 14;14(16):2350.
doi: 10.3390/ani14162350.

Knockdown of Gonadotropin-Releasing Hormone II Receptor Impairs Ovulation Rate, Corpus Luteum Development, and Progesterone Production in Gilts

Amy T Desaulniers  1 , Rebecca A Cederberg  1 , Clay A Lents  2 , Brett R White  1
Affiliations

Knockdown of Gonadotropin-Releasing Hormone II Receptor Impairs Ovulation Rate, Corpus Luteum Development, and Progesterone Production in Gilts

Amy T Desaulniers et al. Animals (Basel). .

Abstract

Reproduction is classically controlled by gonadotropin-releasing hormone (GnRH-I) and its receptor (GnRHR-I) within the brain. In pigs, a second form (GnRH-II) and its specific receptor (GnRHR-II) are also produced, with greater abundance in peripheral vs. central reproductive tissues. The binding of GnRH-II to GnRHR-II has been implicated in the autocrine/paracrine regulation of gonadal steroidogenesis rather than gonadotropin secretion. Blood samples were collected from transgenic gilts, with the ubiquitous knockdown of GnRHR-II (GnRHR-II KD; n = 8) and littermate controls (n = 7) at the onset of estrus (follicular) and 10 days later (luteal); serum concentrations of 16 steroid hormones were quantified by high-performance liquid chromatography tandem mass spectrometry (HPLC-MS/MS). Upon euthanasia, ovarian weight (OWT), ovulation rate (OR), and the weight of each excised Corpus luteum (CLWT) were recorded; HPLC-MS/MS was performed on CL homogenates. During the luteal phase, serum progesterone concentration was reduced by 18% in GnRHR-II KD versus control gilts (p = 0.0329). Age and weight at puberty, estrous cycle length, and OWT were similar between lines (p > 0.05). Interestingly, OR was reduced (p = 0.0123), and total CLWT tended to be reduced (p = 0.0958) in GnRHR-II KD compared with control females. Luteal cells in CL sections from GnRHR-II KD gilts were hypotrophic (p < 0.0001). Therefore, GnRH-II and its receptor may help regulate OR, CL development, and progesterone production in gilts.

Keywords: Corpus luteum; GnRH-II; GnRH-II receptor; autocrine/paracrine regulation; gene knockdown; ovulation rate; porcine; progesterone; steroid hormone.

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Conflict of interest statement

The authors declare no conflicts of interest. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. The USDA prohibits discrimination in all its programs and activities on the basis of race, color, national origin, age, disability, and where applicable, sex, marital status, familial status, parental status, religion, sexual orientation, genetic information, political beliefs, reprisal, or because all or part of an individual’s income is derived from any public assistance program (not all prohibited bases apply to all programs.). Persons with disabilities who require alternative means for the communication of program information (braille, large print, audiotape, etc.) should contact USDA’s TARGET Center at (202) 720-2600 (voice and TDD). To file a complaint of discrimination, write to USDA, Director, Office of Civil Rights, 1400 Independence Avenue, S.W., Washington, DC 20250-9410, or call (800) 795-3272 (voice) or (202) 720-6382 (TDD). USDA is an equal opportunity provider and employer.

Figures

Figure 1
Figure 1
Experimental design. The once daily detection of estrus began at approximately 170 d of age. Puberty was considered the first display of behavioral estrus. The detection of estrus continued for a total of five consecutive estrous cycles. At the onset of the third estrous cycle (d 0), blood was collected via jugular venipuncture (follicular sample) and 10 d later (luteal sample). Animals were euthanized and reproductive tissues were collected on approximately day 7 of the fifth estrous cycle.
Figure 2
Figure 2
Body weights were not different between GnRHR-II KD (n = 8) and littermate control (n = 7) gilts over time. Body weight was recorded at birth, weaning, and during pre-pubertal development (40, 60, 80, 100, 125, 145 and 165 d of age). Results are presented as least squares means (LSMEANS) ± the standard error of the mean (SEM). Line, p = 0.3677; Age, p < 0.0001; Line × Age, p = 0.7960.
Figure 3
Figure 3
Age at puberty (a), weight at puberty (b), and estrous cycle length (c) in GnRHR-II KD (n = 8) and littermate control (n = 7) gilts. No line effects were detected (p > 0.10). Results are presented as least squares means (LSMEANS) ± the standard error of the mean (SEM).
Figure 4
Figure 4
Concentrations of 11-deoxycortisol in blood serum samples from GnRHR-II KD (n = 8) and littermate control (n = 7) gilts during the follicular and luteal phases of the estrous cycle. There was no effect of phase or line by phase interaction (p > 0.05). However, there was an overall effect (p = 0.0320) of line; GnRHR-II KD gilts had reduced circulating concentrations. Results are presented as least squares means (LSMEANS) ± the standard error of the mean (SEM). * p < 0.05.
Figure 5
Figure 5
Progestogen concentrations in blood serum samples from GnRHR-II KD (n = 8) and littermate control (n = 7) gilts during the follicular and luteal phase of the estrous cycle. Neither an effect of line (GnRHR-II KD versus control) nor a line by phase interaction was detected for 17α-hydroxyprogesterone, so these data are not reported. However, a phase effect (p = 0.0006) was detected for 17α-hydroxyprogesterone, with the concentration greater during the luteal phase (a). A line by phase interaction (p = 0.0341) was detected for progesterone; GnRHR-II KD gilts produced less progesterone during the luteal phase (b). Results are presented as least squares means (LSMEANS) ± the standard error of the mean (SEM). a,b,c Divergent letters differ significantly (p < 0.05); * p < 0.05.
Figure 6
Figure 6
Androgen concentrations during the follicular phase and luteal phase in blood serum samples from GnRHR-II KD (n = 8) and littermate control (n = 7) gilts. No effect of line (GnRHR-II KD versus control) nor line by phase interaction was detected for any androgen examined (p > 0.05); therefore, these data are not reported. A phase effect (p < 0.05) was detected for testosterone (a), androsterone (b) and androstenedione (c) with concentrations greater during the follicular phase. Results are presented as least squares means (LSMEANS) ± the standard error of the mean (SEM). * p < 0.05.
Figure 7
Figure 7
Estrogen concentrations during the follicular and luteal phase in blood serum samples from GnRHR-II KD (n = 8) and littermate control (n = 7) gilts. No effect of line (GnRHR-II KD versus control) nor line by phase interaction was detected for estrogens (p > 0.05); therefore, these data are not reported. A phase effect (p < 0.05) was detected for both 17β-estradiol (a) and estrone (b) with concentrations greater during the follicular phase compared with luteal phase. Results are presented as least squares means (LSMEANS) ± the standard error of the mean (SEM). * p < 0.05.
Figure 8
Figure 8
Ovarian characteristics in GnRHR-II KD (n = 8) and littermate control (n = 7) gilts. Paired ovary weight (a) was similar (p > 0.10) between lines, but ovulation rate (number of Corpora lutea) (b) was reduced (p = 0.0123) in GnRHR-II KD gilts compared with littermate controls. Results are presented as least squares means (LSMEANS) ± the standard error of the mean (SEM). * p < 0.05.
Figure 9
Figure 9
Corpus luteum (CL) metrics and GnRHR-II expression in CL samples from GnRHR-II KD and littermate control gilts. Average individual CL weight was greater (p < 0.0001) in GnRHR-II KD (n = 4) versus control (n = 4) gilts (a). Total CL weight per ovary tended to be reduced (p = 0.0958) in GnRHR-II KD (n = 4) versus control (n = 4) gilts (b). Luteal cell area was reduced (p < 0.0001) in GnRHR-II KD (n = 7) versus littermate control (n = 6) gilts (c). Expression of GnRHR-II tended to be reduced (p = 0.0774) by 21% in CL from GnRHR-II KD (n = 8) versus control (n = 7) gilts (d). Results are presented as least squares means (LSMEANS) ± the standard error of the mean (SEM). * p < 0.05; † p < 0.10.
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