The effect of select seminal plasma proteins on endometrial mRNA cytokine expression in mares susceptible to persistent mating-induced endometritis.
Abstract: In the horse, breeding induces a transient endometrial inflammation. A subset of mares are unable to resolve this inflammation, and they are considered susceptible to persistent mating-induced endometritis PMIE Select seminal plasma proteins cysteine-rich secretory protein-3 (CRISP-3) and lactoferrin have been shown to affect the innate immune response to sperm in vitro. The objective of this study was to determine whether the addition of CRISP-3 and lactoferrin at the time of insemination had an effect on the mRNA expression of endometrial cytokines in susceptible mares after breeding. Six mares classified as susceptible to PMIE were inseminated during four consecutive oestrous cycles with treatments in randomized order of: 1 mg/ml CRISP-3, 150 μg/ml lactoferrin, seminal plasma (positive control) or lactated Ringer's solution (LRS; negative control) to a total volume of 10 ml combined with 1 × 10 spermatozoa pooled from two stallions. Six hours after treatment, an endometrial biopsy was obtained for qPCR analysis of selected genes associated with inflammation (pro-inflammatory cytokines interleukin (IL)-1β, IL-8, tumour necrosis factor (TNF)-α, interferon (INF)-γ, anti-inflammatory cytokines IL-1RN and IL-10, and inflammatory-modulating cytokine IL-6). Seminal plasma treatment increased the mRNA expression of IL-1β (p = .019) and IL-8 (p = .0068), while suppressing the mRNA expression of TNF (p = .0013). Lactoferrin also suppressed the mRNA expression of TNF (p = .0013). In conclusion, exogenous lactoferrin may be considered as one modulator of the complex series of events resulting in the poorly regulated pro-inflammatory response seen in susceptible mares.
© 2016 Blackwell Verlag GmbH.
Publication Date: 2016-09-30 PubMed ID: 27686063DOI: 10.1111/rda.12813Google Scholar: Lookup
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- Journal Article
Summary
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This study investigates how certain seminal plasma proteins can impact the expression of cytokine genes in the endometrial lining of mares susceptible to persistent mating-induced endometritis (PMIE), a type of inflammation caused by breeding. The researchers found that adding lactoferrin at the time of insemination reduced the expression of specific inflammation-related genes, suggesting it could be used to moderate the inflammation response in susceptible mares.
Research Context
- In horses, breeding often leads to short-term inflammation in the endometrial lining. However, a subset of mares suffer from persistent inflammation known as PMIE (Persistent Mating-Induced Endometritis).
- Previous research has identified two seminal proteins – CRISP-3 (cysteine-rich secretory protein-3) and lactoferrin – as having the capacity to influence the innate immune response to sperm in laboratory conditions.
Methodology
- In this study, six mares identified as susceptible to PMIE were inseminated across four continuous oestrous cycles using four different treatments: CRISP-3, lactoferrin, seminal plasma (as a positive control), and lactated Ringer’s solution (as a negative control).
- The treatments were administered in a randomized order at the time of insemination, combined with sperm from two different stallions.
- An endometrial biopsy was taken six hours after insemination for analysis of the expression of certain genes linked to inflammation.
Results
- Seminal plasma treatment increased the gene expression of Interleukin (IL)-1β and IL-8, two inflammation-promoting cytokines. Additionally, it suppressed the expression of TNF (tumour necrosis factor), another cytokine that plays a major role in inflammation.
- Lactoferrin treatment also suppressed the gene expression of TNF.
Conclusion
- The results of the study suggest that lactoferrin, when added at the time of insemination, can influence the expression of inflammation-related genes in a way that might help to moderate the inflammatory response in mares susceptible to PMIE.
- Therefore, lactoferrin could possibly be considered as a means to improve the regulation of the inflammatory response in these mares.
Cite This Article
APA
Fedorka CE, Scoggin KE, Woodward EM, Squires EL, Ball BA, Troedsson M.
(2016).
The effect of select seminal plasma proteins on endometrial mRNA cytokine expression in mares susceptible to persistent mating-induced endometritis.
Reprod Domest Anim, 52(1), 89-96.
https://doi.org/10.1111/rda.12813 Publication
Researcher Affiliations
- Department of Veterinary Science, College of Agriculture Food and Environment, University of Kentucky, Lexington, KY, USA.
- Department of Veterinary Science, College of Agriculture Food and Environment, University of Kentucky, Lexington, KY, USA.
- Department of Clinical Sciences, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA, USA.
- Department of Veterinary Science, College of Agriculture Food and Environment, University of Kentucky, Lexington, KY, USA.
- Department of Veterinary Science, College of Agriculture Food and Environment, University of Kentucky, Lexington, KY, USA.
- Department of Veterinary Science, College of Agriculture Food and Environment, University of Kentucky, Lexington, KY, USA.
MeSH Terms
- Animals
- Breeding
- Cytokines / genetics
- Cytokines / metabolism
- Endometritis / pathology
- Endometritis / veterinary
- Endometrium / pathology
- Estrous Cycle / immunology
- Female
- Horse Diseases / pathology
- Horses / genetics
- Insemination, Artificial / veterinary
- Lactoferrin / genetics
- Male
- RNA, Messenger / genetics
- Random Allocation
- Semen / metabolism
- Seminal Plasma Proteins / genetics
Citations
This article has been cited 6 times.- Gardela J, Ruiz-Conca M, Wright D, López-Béjar M, Martínez CA, Rodríguez-Martínez H, Álvarez-Rodríguez M. Semen Modulates Cell Proliferation and Differentiation-Related Transcripts in the Pig Peri-Ovulatory Endometrium. Biology (Basel) 2022 Apr 18;11(4).
- Morgan HL, Eid N, Khoshkerdar A, Watkins AJ. Defining the male contribution to embryo quality and offspring health in assisted reproduction in farm animals. Anim Reprod 2020 Aug 5;17(3):e20200018.
- Recuero S, Sánchez JM, Mateo-Otero Y, Bagés-Arnal S, McDonald M, Behura SK, Spencer TE, Kenny DA, Yeste M, Lonergan P, Fernandez-Fuertes B. Mating to Intact, but Not Vasectomized, Males Elicits Changes in the Endometrial Transcriptome: Insights From the Bovine Model. Front Cell Dev Biol 2020;8:547.
- Canisso IF, Segabinazzi LGTM, Fedorka CE. Persistent Breeding-Induced Endometritis in Mares - a Multifaceted Challenge: From Clinical Aspects to Immunopathogenesis and Pathobiology. Int J Mol Sci 2020 Feb 20;21(4).
- Johannisson A, Al-Essawe EM, Al-Saffar AK, Karkehabadi S, Lima-Verde I, Wulf M, Aurich C, Morrell JM. Season does not have a deleterious effect on proportions of stallion seminal plasma proteins. J Reprod Dev 2020 Jun 12;66(3):215-221.
- Shen Q, Wu X, Chen J, He C, Wang Z, Zhou B, Zhang H. Immune Regulation of Seminal Plasma on the Endometrial Microenvironment: Physiological and Pathological Conditions. Int J Mol Sci 2023 Sep 27;24(19).
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