Source: WEST VIRGINIA UNIVERSITY submitted to NRP
ESTROGENIC REGULATION OF LH SECRETION IN PREPUBERTAL EWES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1028207
Grant No.
2022-67011-36631
Cumulative Award Amt.
$106,000.00
Proposal No.
2021-09384
Multistate No.
(N/A)
Project Start Date
Jan 1, 2022
Project End Date
Dec 31, 2023
Grant Year
2022
Program Code
[A7101]- AFRI Predoctoral Fellowships
Recipient Organization
WEST VIRGINIA UNIVERSITY
886 CHESTNUT RIDGE RD RM 202
MORGANTOWN,WV 26505-2742
Performing Department
Physiology and Pharmacology
Non Technical Summary
Within the body, a part of the brain called the hypothalamus releases the hormone, gonadotropin releasing hormone (GnRH). This acts on the pituitary to release luteinizing hormone (LH), which acts on the ovaries to release estradiol (E2). E2then feeds back in a negative manner and inhibits the release of GnRH and LH. In many mammal species, as they reachpuberty, there is a decrease in the inhibition by E2, leading to an increase of GnRH and LH, which eventually leads to puberty onset. It is currently unknown what causes this change in E2-negative feedback, and therefore what controls the timing of puberty onset. Adding to the complexity, E2cannot act directly tosuppress GnRH, since the neurons that release GnRH lack receptors for estradiol, ERa. This means that there must be other neurons that haveERa and which acton GnRH neurons.Delayedpuberty onset in domestic animals leads to a decrease in lifetime productivity of the animal, therefore decreasing profitability for producers. In addition, delayed puberty in humans has a number of negative effects on health. Determining what mechanisms control the timing of puberty onset may allow for more options to address these issues.The first goal of this project is to determine where in the hypothalamus estradiol is acting. The first experiment involves placingE2in specific areas of the hypothalamus, namely either the preoptic area (POA) or the arcuate nucleus (ARC), of ewesafter removing the ovaries, and therefore any circulating estradiol. Blood samples will then be taken to determine if the E2implants reduce LH, indicating that E2is acting in either the POA or ARC (or both), or if there is no response. The second experiment will involve placing ICI, a compound that blocks the receptor for E2, in either the POA or ARC of ewes. The ovaries of the ewes will be removed, but E2will be givenso that there is a constant amount of estradiol in circulation. Blood samples will be taken to determine if the results supportthe first experiment, i.e., if E2is acting in that area, the ICI compound should block it from working and the LH levels will be increased.The second goal of the proposal is to try to determine the neurons in the hypothalamusthat act onGnRH neurons and thatmay be responsible for the change in E2-negative feedback that leads to puberty. We have identified a few populations of cells that we know act on GnRH in some way: ARC propiomelantocortin (POMC) neurons, ARC agouti-related peptide (AgRP) neurons, and POA NK3R-containing neurons. POMC and AgRP neurons are known to have ERa receptors. Approaches will be used that will enable us to assess changes in the number ofPOMC, AgRP and NK3R neurons with pubertal development as well as whether ERa expression in each of these different sets of neurons changes.If ERa expression one or more of these sets of neurons changes, then it might suggest that they are involved in the change in E2-negative feedback that leads to puberty onset.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
30136101020100%
Knowledge Area
301 - Reproductive Performance of Animals;

Subject Of Investigation
3610 - Sheep, live animal;

Field Of Science
1020 - Physiology;
Goals / Objectives
The normal timing of puberty onset in domestic livestock is critical for maximal productivity and, therefore, profitabilityfor the producer. Puberty onset is caused by an increase in gonadotropin releasing hormone (GnRH) secretion, and, in turn, luteinizing hormone (LH),as a result of decreased estradiol (E2) negative feedback. GnRH neurons, located in the preoptic area of the hypothalamus, lack the receptors for estradiol, ERa. This indicates that the shift in E2negative feedback must happenin neurons afferent to GnRH neurons. It is currently unknown in what neurons or where this occurs. Aim 1 of this project is to determine if E2 acts within the preoptic area (POA) or the arcuate nucleus (ARC) of the hypothalamusto inhibit(LH)secretion in prepubertal female lambs. Thiswill be done by applying E2or blocking E2in those areas. Aim 2 of thisproposal focuses on defining changes in neuronal populations that contain ERaover development. Within the ARC, the neuronal populations targeted will be propiomelanocortin (POMC) neurons and agouti-related peptide (AgRP) neurons. Within the POA, the focus will be on neurons containing NK3R, the receptor for neurokinin B.
Project Methods
The first experiment conducted will involve ovariectomizing a group of ewes and placing guide cannulas in either the POA or the ARC. After a two week recovery, blood samples will be collected every 12 minutes for four hours, then assessed for LH using a radioimmunoassay. After this, the ewes will receive either a blank implant or an estradiol implant within the cannula for each area. After a week, blood samples will be collected using the same method. Treatments will then be reversed in a crossover design, allowing each animal to serve as its owncontrol.One week later, blood samples will be collected again, after which hypothalamic tissue will be collected. Blood samples will be analyzed for LH pulses using the following criteria:(1) a peak within two samples of the previous nadir; (2) amplitude greater than sensitivity of the LH assay; and (3) three standard deviations larger than the nadir directly preceding and following it. The hypothalamic tissue will be visualized with H&E staining to determine if the guide cannulas were placed in the proper region of the hypothalamus.The second experiment will also involveovariectomizing a group of ewes and placing guide cannulas in either the POA or the ARC, however E2implants will be placed subcutaneously in the ewes at the time of ovariectomy. After atwo week recovery, blood samples will be collected every 12 minutes for four hours, then run for LH using a radioimmunoassay. After this, the ewes will receive either a blank implant or an ICI implant, an ERa antagonist, within each targeted area. A week later, blood samples will be collected, and treatments will be reversed in a crossover design. One week later, blood samples will be collected again and the blank, ICI, and E2implants will be removed. One week later, a final blood collection will be performed and hypothalamic tissue will be collected. The same analyses forpulsatile LH secretion and guide cannula placement will be performed as for experiment 1.In the third experiment, hypothalamic tissue from ewes aged 5 months (prepubertal), 8 months (peripubertal), and 10 months (postpubertal) will be assessed using immunohistochemistry. ARC tissue will be stained for POMC and ERa, and AgRP and ERa. POA tissue will be stained for NK3R and ERa. The number of cell bodies containing each neuropeptide and the percentage colocalization with ERa at each stage of pubertal development will be analyzed using an Olympus Slide Scanner to visualizecells andOlyvia to perform quantitative analyses.

Progress 01/01/22 to 12/31/23

Outputs
Target Audience:Data was presented periodically throughout the study to faculty and students, both graduate and undergraduate, of the Physiology and Pharmacology department at West Virginia University. Data was presented to a larger audience of scientists at the national meeting of the Society for Neuroscience conference in Washington D.C.in November 2023 andthe Endocrine Society meeting in June 2023. Publication summarizing the work is currently underway. Changes/Problems:Originally, we planned to assess the percent of POA NK3R cells that were ERα positive. However, due to issues obtaining materials, namely more of the ERαantibody, we have decided to remove this from the project. Preliminary data suggested that there was no colocalization between the two, so the materials we had were prioritized for the other aspects of the project. What opportunities for training and professional development has the project provided?The PD has had the opportunity to learn how to organize and ensure that neurosurgeries run smoothly, as well as develop her neurosurgical techniques. The PD also attended three in-person conferences to present data, developposter presentation skills and networkwith other scientists. This has assisted with her postdoctoral position search. A master's student joined the lab during the course of this project, and the PD has been given the chance to develop more mentorship skilss as she teaches her new techniques and analysis. The PD took an experimental design class and has been able to put those skills to practical use while analyzing data for this project. The PD has significantly improved her writing skills while preparing manuscripts to publish the data collected during this project. How have the results been disseminated to communities of interest?Results from these studies have been presented in oral format at department-wide seminars, as well as in lab meetings. The results have also been shown to scientists at other universities through postdoctoral interview seminars. The data has been shown at national conferences as well. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Aim 1 of this project was to determine if estradiol (E2) acts within the preoptic area (POA) or the arcuate nucleus (ARC) of the hypothalamus inhibit LH secretion in prepubertal female lambs. Experiment 1 was completed: 6 ewes were implanted with E2 microimplants in the ARC, and8 ewes were implanted with E2 microimplants in the POA. Results of LH assays determined that there was incomplete inhibition of LH with both sets of ewes, indicating that the two areas work in tandem to modulate E2 signals. However, it appeared that the inhibition was more complete in the ARC implanted ewes, suggesting that this area may be more important for regulation. Experiment 2 was also completed: 6 ewes were implanted with the receptor for E2, ERα, antagonists within the POA, and 5 ewes were implanted with ERα antagonists in the ARC. Blood samples taken from this experiment are currently under assessment for LH levels, and we expect to have this completed and published within the year. Aim 2of this project wasto determine the changes in neuronal populations that contain ERα over development. Staining has been completed and analyzed to determine the percent of the propiomelanocortin (POMC) and agouti-related peptide (AgRP) populations in the ARC that are ERα positive through development. We determined that around 30-40% of ARC POMC neurons are ERα positive, and that there is no significant change in this through pubertal development. We also determined that around 30% of ARC AgRP neurons are ERα positive. We have also determined that there isno significant change in this through pubertal development. We are currently undergoing more staining to increase the sample size for this analysis.

Publications

  • Type: Journal Articles Status: Published Year Published: 2023 Citation: Aerts, E. G., Griesgraber, M. J., Shuping, S. L., Bowdridge, E. C., Hardy, S. L., Goodman, R. L., Nestor, C. C., & Hileman, S. M. (2023). The effect of NK3-Saporin injection within the arcuate nucleus on puberty, the LH surge, and the response to Senktide in female sheep. Biology of reproduction, ioad147. Advance online publication. https://doi.org/10.1093/biolre/ioad147
  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: The Role of the Melanocortin System in Ovine Puberty. Poster ⿿ Endocrine Society, Chicago, IL, 2023.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Investigation into the role of estradiol in puberty onset of female sheep. Poster ⿿ Society for Neuroscience, Washington D.C., 2023.


Progress 01/01/22 to 12/31/22

Outputs
Target Audience:Data was presented periodically throughout the study to faculty and students, both graduate and undergraduate, of the Physiology and Pharmacology department at West Virginia University. Data was presented to a larger audienceof scientists at the national meeting of the Society for Neuroscience conference in San Diego in November 2022. Data is also being prepared for presentation at the Endocrine Society meeting andpublication in the coming year. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The PD has had the opportunity to learn how to organize and ensure thatneurosurgeries run smoothly, as well as develop her neurosurgical techniques. The PD also attended her first in-person conference to present data, developing poster presentation skills and networking with other scientists. A masters student has joined the lab, whom the PD has been mentoring. The PD has also been afforded the opportunity to prepare data for manuscripts, oral presentations, and poster presentations. She has also been assisting with manuscript preparation and learning the associated skills. In addition to being exposed to the statistical analyses analyzing their data provides, the PD is also taking an experimental design class. How have the results been disseminated to communities of interest?Results from these studies have been presented in oral format at department-wide seminars, as well as in lab meetings. What do you plan to do during the next reporting period to accomplish the goals?Results from all of the previous work will be analyzed and preparedfor presentation and publication. Tissue will be used to complete the examination in changes of ERalpha and AgRP over development using either immunohistochemistry or RNAScope, as well as the changes in ERalpha and NK3R using RNAScope. Sixteen sheep will receive guide cannulas in either the POA or ARC and receive an ER-alphainhibitor to determine where in the hypothalamus E2is acting.

Impacts
What was accomplished under these goals? Aim 1of this proposal focuses on determining if E2acts within the POA or the ARC of the hypothalamus to inhibit LH secretion in prepubertal female lambs. Since receiving this grant, we have completed the first round of experiments to test where E2is acting by implanting E2microimplants in the POA or ARC of ovariectomized ewes and determining their LH levels. Sixewes were implanted with permanent guide cannulas in the ARC and eightewes were implanted in the POA. Blood samples were taken a week after implantation, a week after E2microimplants were inserted, and a week after subcutaneous E2was placed.We are currently waiting for the results from LH radioimmunoassays, and then will begin data analysis. Aim 2of this proposal is to determine the changes in neuronal populations that contain ERalpha over development. Aprotocol for a dual label immunohistochemical stain of ER-alpha and POMChas been developed and optimized. We are currently performing dual-label immunochemical staining to assess staining in ER-alpha within POMC neurons during pubertal development.

Publications