Mating induces early transcriptional response in the rat endosalpinx: the role of TNF and RA

in Reproduction
Authors:
Lidia M Zúñiga Laboratorio de Bioquímica, Departamento Biomédico, and Centre for Biotechnology and Bioengineering (CeBiB), Universidad de Antofagasta, Antofagasta, Chile

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Juan-Carlos Andrade Laboratorio de Biología de la Reproducción, Instituto Antofagasta, Universidad de Antofagasta, Antofagasta, Chile

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Francisca Fábrega-Guerén Laboratorio de Bioquímica, Departamento Biomédico, and Centre for Biotechnology and Bioengineering (CeBiB), Universidad de Antofagasta, Antofagasta, Chile

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Pedro A Orihuela Laboratorio de Inmunología de la Reproducción, Facultad de Química y Biología, Universidad de Santiago de Chile, Santiago, Chile

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https://orcid.org/0000-0002-4238-0932
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Ethel V Velásquez Departamento de Tecnologías Nucleares, Comisión Chilena de Energía Nuclear, Santiago, Chile

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Elena A Vidal Centro de Genómica y Bioinformática, Facultad de Ciencias, Universidad Mayor, Santiago, Chile
ANID, Programa Iniciativa Científica Milenio, Millennium Institute for Integrative Biology iBio, Santiago, Chile

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Rodrigo A Gutiérrez FONDAP Centre for Genome Regulation, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
ANID, Programa Iniciativa Científica Milenio, Millennium Institute for Integrative Biology iBio, Santiago, Chile

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Patricio Morales Laboratorio de Biología de la Reproducción, Instituto Antofagasta, Universidad de Antofagasta, Antofagasta, Chile

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Benito Gómez-Silva Laboratorio de Bioquímica, Departamento Biomédico, and Centre for Biotechnology and Bioengineering (CeBiB), Universidad de Antofagasta, Antofagasta, Chile

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Horacio B Croxatto Instituto de Salud Pública, Facultad de Medicina, Universidad Andrés Bello, Santiago, Chile

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Correspondence should be addressed to L M Zúñiga or H B Croxatto; Email: lidia.zuniga@uantof.cl or horacio.croxatto@unab.cl
DOI:
https://doi.org/10.1530/REP-20-0190
Volume/Issue:
Volume 161: Issue 1
Page Range:
43–59
Article Type:
Research Article
Online Publication Date:
Jan 2021
Copyright:
© 2021 Society for Reproduction and Fertility 2021
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During mating, males provide not only the spermatozoa to fertilize the oocyte but also other stimuli that are essential for initiating and maintaining the reproductive programme in females. In the mammalian oviduct, mating regulates sperm storage, egg transport, fertilization, early embryonic development, and oestradiol metabolism. However, the main molecules underlying these processes are poorly understood. Using microarray analyses, we identified 58 genes that were either induced or repressed by mating in the endosalpinx at 3 h post-stimulus. RT-qPCR confirmed that mating downregulated the expression of the Oas1h and Prim1 genes and upregulated the expression of the Ceacam1, Chad, Chst10, Slc5a3 and Slc26a4 genes. The functional category ‘cell-to-cell signalling and interaction’ was over-represented in this gene list. Network modelling identified TNF and all-trans retinoic acid (RA) as upstream regulators of the mating-induced transcriptional response, which was confirmed by intraoviductal injection of TNF or RA in unmated rats. It partially mimicked the transcriptional effect of mating in the rat endosalpinx. Furthermore, mating decreased RA levels in oviductal fluid, and RA-receptor-gamma (RARG) exhibited a nuclear location in oviductal epithelium in both unmated and mated rats, indicating RA-RARG transcriptional activity. In conclusion, the early transcriptional response regulated by mating in the rat endosalpinx is mediated by TNF and RA. These signalling molecules regulate a cohort of genes involved in ‘cell-to-cell signalling and interactions’ and merit further studies to understand the specific processes activated in the endosalpinx to sustain the events that occur in the mammalian oviduct early after mating.

Supplementary Materials

    • Supplementary Table 1. Genes observed to be upregulated in rat endosalpinx by mating, as identified by microarray analysis. We used the Rat Gene 1.0 ST Array from Affymetrix. The RankProd package was used for the identification of differentially expressed genes using a p-value cut-off = 0.001. Then, the list of upregulated genes was selected using a PFP cut-off = 0.1 (horizontal line in table). RP: Rank Product; PFP: Percentage of false positives. FC: Fold Change.
    • Supplementary Table 2. Genes observed to be downregulated in rat endosalpinx by mating, as identified by microarray analysis. We used the Rat Gene 1.0 ST Array from Affymetrix. The RankProd package was used for the identification of differentially expressed genes using a p-value cut-off = 0.001. Then, the list of downregulated genes was selected using a PFP cut-off = 0.1 (horizontal line in table). RP: Rank Product; PFP: Percentage of false positives. FC: Fold Change.
    • Supplementary Table 3. Networks predicted by IPA involving mating-regulated genes in rat endosalpinx. Genes were identified by microarray analysis, with only 19 of the 24 genes identified by IPA included in the 5 networks. Key of molecules in the networks: gene symbols from human, all letters capitalised; gene symbols from mouse and rat, first letter capitalised; other molecules, letters in roman (i.e. not italicised); and genes highlighted in bold are focus molecules.
    • Supplementary Table 4. NormFinder analysis for the best combination of reference genes.
    • Supplementary Table 5. qPCR conditions tested for primers with lower detection or amplification specificity issues in endosalpinx samples.
    • Supplementary Table 6. Unique network predicted by IPA involving TNF and mating-regulated genes in rat endosalpinx. Key of molecules in the network: gene symbols from human, all letters capitalised; gene symbols from mouse and rat, first letter capitalised; other molecules, letters in roman (i.e. not italicised); and genes highlighted in bold are focus molecules.
    • Supplementary Fig. 1 RNA integrity analysis.
    • Supplementary Fig. 2 (A – B)
    • Supplementary Fig. 3 Key of relationships.
    • Supplementary Fig. 4 (A – D) RT-qPCR amplification specificity.
    • Supplementary Fig. 5 (A – B) Agarose gel analysis of RT-qPCR amplification.
    • Supplementary Fig. 6 (A – B) RT-qPCR amplification efficiency.

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1470-1626
Online ISSN:
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