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Biology of reproduction2002; 67(2); 630-636; doi: 10.1095/biolreprod67.2.630

Expression of interleukin-1 (IL-1) system genes in equine cumulus-oocyte complexes and influence of IL-1beta during in vitro maturation.

Abstract: A growing body of evidence suggests that the ovary is a site of inflammatory reactions, and thus, ovarian cells could represent sources and targets of the interleukin-1 (IL-1) system. The aim of the present work was to investigate the expression of IL-1alpha, IL-1beta, IL-1ra, IL-1R1, and IL-1R2 genes in equine cumulus cells and oocytes. Moreover, the influence of IL-1beta on in vitro maturation of cumulus-oocytes complexes (COCs) was examined. COCs were collected using ultrasound-guided follicular puncture in vivo. Oocytes and cumulus cells were isolated from preovulatory and subordinate follicles and were analyzed either at collection or after in vitro culture. An ultrasensitive reverse transcription-polymerase chain reaction was used to study the expression of IL-1 system members. In order to study the in vitro effect of IL-1beta on oocyte nuclear maturation and cumulus expansion, immature COCs collected from subordinate follicles were cultured for 30 h in media containing or not containing IL-1beta alone, or in combination with equine luteinizing hormone. Our results indicated that equine oocytes expressed IL-1beta and IL-1R2 genes, and that cumulus cells expressed all IL-1 system members except IL-1alpha. In oocytes, IL-1beta expression significantly decreased during in vitro culture compared with immature and mature oocytes analyzed at collection. Similarly, in cumulus cells, in vitro culture decreased IL-1ra and IL-1R1 expression. IL-1beta was shown to significantly decrease the gonadotropin-induced nuclear maturation of oocytes. In conclusion, we demonstrated for the first time, in mares, the presence of IL-1beta and IL-1R2 transcripts in oocytes and of IL-1beta, IL-1ra, IL-1R1, and IL-1R2 in cumulus cells. The regulatory effect of IL-1beta on COCs during maturation suggests that the IL-1 system could be of crucial importance for ovarian physiology in the mare.
Publication Date: 2002-07-24 PubMed ID: 12135907DOI: 10.1095/biolreprod67.2.630Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

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This research explores the presence and role of certain interleukin-1 (IL-1) system genes within horse oocytes and cumulus cells. It found that IL-1beta, a particular gene within this system, could significantly affect the maturation process of cumulus-oocyte complexes (COCs) in horses, indicating a potential key role of the IL-1 system in ovarian physiology.

Expression of IL-1 System Genes

  • The research aimed to investigate the expression (or presence) of a range of IL-1 system genes – specifically IL-1alpha, IL-1beta, IL-1ra, IL-1R1, and IL-1R2 – within horse cumulus cells and oocytes. These are types of cells found within the ovary.
  • The COCs were collected in vivo, from preovulatory and subordinate follicles, and looked at both upon collection and after in vitro (test tube) culture.
  • Researchers found that oocytes expressed IL-1beta and IL-1R2 genes, whereas cumulus cells expressed every investigated IL-1 system member except IL-1alpha.

The Influence of IL-1beta

  • In addition to identifying which IL-1 system genes were expressed in the cumulus cells and oocytes, the study also examined how one particular gene, IL-1beta, influences the in vitro maturation of COCs.
  • To do this, the researchers cultured immature COCs from subordinate follicles for 30 hours in media either containing or not containing IL-1beta alone, or together with equine luteinizing hormone.
  • The results revealed a significant decrease in IL-1beta expression in oocytes during the in vitro culture compared to both immature and mature oocytes analysed at collection.
  • Notably, the presence of IL-1beta was shown to significantly inhibit the gonadotropin-induced nuclear maturation of oocytes, suggesting that it has a significant regulatory impact on COC maturation.

Conclusion

  • In short, this research identifies the presence of various IL-1 system genes within horse oocytes and cumulus cells, as well as the significant influence of IL-1beta on the maturation of COCs.
  • The findings indicate the potential importance of the IL-1 system for ovarian physiology in horses, shedding new light on the mechanisms influencing ovary function.

Cite This Article

APA
Martoriati A, Lalmanach AC, Goudet G, Gérard N. (2002). Expression of interleukin-1 (IL-1) system genes in equine cumulus-oocyte complexes and influence of IL-1beta during in vitro maturation. Biol Reprod, 67(2), 630-636. https://doi.org/10.1095/biolreprod67.2.630

Publication

ISSN: 0006-3363
NlmUniqueID: 0207224
Country: United States
Language: English
Volume: 67
Issue: 2
Pages: 630-636

Researcher Affiliations

Martoriati, Alain
  • Institut National de la Recherche Agronomique-Haras Nationaux, Equipe de Reproduction Equine, P.R.C., F-37380 Nouzilly, France.
Lalmanach, Anne-Christine
    Goudet, Ghylène
      Gérard, Nadine

        MeSH Terms

        • Animals
        • Cell Nucleus / genetics
        • Cell Nucleus / ultrastructure
        • Female
        • Fertilization in Vitro
        • Gene Expression Regulation / genetics
        • Horses / physiology
        • In Situ Hybridization
        • Interleukin-1 / genetics
        • Meiosis / drug effects
        • Oocytes / growth & development
        • Oocytes / physiology
        • Ovary / cytology
        • Ovary / physiology
        • Pregnancy
        • RNA, Messenger / biosynthesis
        • Reverse Transcriptase Polymerase Chain Reaction

        Citations

        This article has been cited 5 times.
        1. Wen X, Yang Q, Sun D, Jiang ZY, Wang T, Liu HR, Han Z, Wang L, Liang CG. Cumulus Cells Accelerate Postovulatory Oocyte Aging through IL1-IL1R1 Interaction in Mice. Int J Mol Sci 2023 Feb 9;24(4).
          doi: 10.3390/ijms24043530pubmed: 36834943google scholar: lookup
        2. Popovic M, Sartorius G, Christ-Crain M. Chronic low-grade inflammation in polycystic ovary syndrome: is there a (patho)-physiological role for interleukin-1?. Semin Immunopathol 2019 Jul;41(4):447-459.
          doi: 10.1007/s00281-019-00737-4pubmed: 31139895google scholar: lookup
        3. Caillaud M, Duchamp G, Gérard N. In vivo effect of interleukin-1beta and interleukin-1RA on oocyte cytoplasmic maturation, ovulation, and early embryonic development in the mare. Reprod Biol Endocrinol 2005 Jun 22;3:26.
          doi: 10.1186/1477-7827-3-26pubmed: 15972098google scholar: lookup
        4. Dell'Aquila ME, Caillaud M, Maritato F, Martoriati A, Gérard N, Aiudi G, Minoia P, Goudet G. Cumulus expansion, nuclear maturation and connexin 43, cyclooxygenase-2 and FSH receptor mRNA expression in equine cumulus-oocyte complexes cultured in vitro in the presence of FSH and precursors for hyaluronic acid synthesis. Reprod Biol Endocrinol 2004 Jun 22;2:44.
          doi: 10.1186/1477-7827-2-44pubmed: 15212696google scholar: lookup
        5. Martoriati A, Gérard N. Interleukin-1 (IL-1) system gene expression in granulosa cells: kinetics during terminal preovulatory follicle maturation in the mare. Reprod Biol Endocrinol 2003 May 16;1:42.
          doi: 10.1186/1477-7827-1-42pubmed: 12803652google scholar: lookup