Porcine-specific expression of the three functional CYP19 paralogs in early conceptus, placenta, and gonads

in Reproduction
Authors:
Caroline Gomes Lucas Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America

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Riley M Sullivan Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America

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Caroline A Pfeiffer Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America

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Paula R Chen Department of Agriculture - Agricultural Research Service, Plant Genetics Research Unit, Columbia, Missouri, USA

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JaeWoo Kim Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America

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Mariana Sponchiado Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America

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Alan J Conley Department of Population Health and Reproduction, School of Veterinary Medicine, University of California at Davis, Davis, California, USA

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Randall S Prather Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America

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Kevin D Wells Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America

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Rodney D Geisert Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America

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Correspondence should be addressed to C Gomes Lucas; Email: lucascg@missouri.edu
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In brief

Aromatase catalyzes the synthesis of estrogens and has been shown to have an important role during the establishment of pregnancy in the pig. This study confirmed the differential expression of the three aromatase isoforms.

Abstract

Although three porcine aromatase isoforms have been identified, their gene expression profiles in reproduction are still poorly understood. Here, we identified by Sanger sequencing unique nucleotide signatures for the three paralogous copies of Cyp19 and analyzed by RT-PCR the occurrence of the Cyp19 and Cyp17a1 transcripts at different tissues and stages of conceptus and fetal–placental development. Cyp19a1 and Cyp19a3 expressions were detected in conceptuses and gonads, respectively. Cyp19a2 transcripts were identified on both the conceptuses and the placenta samples. Transcripts for Cyp17a1 were detected predominantly in conceptus and gonads. In the endometrium of day 21 pregnant females, as well as days 12 and 17 pseudopregnant females, we did not detect the expression of Cyp19a1, Cyp19a2, or Cyp19a3. In our study, we have demonstrated distinct transcriptional regulation for the three functional Cyp19 paralogs and a potential role for Cyp17a1 in controlling the secretion of estrogen from the conceptus and the placenta.

 

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  • Bazer FW & & Johnson GA 2014 Pig blastocyst–uterine interactions. Differentiation; Research in Biological Diversity 87 5265. (https://doi.org/10.1016/J.DIFF.2013.11.005)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chen X, Li A, Chen W, Wei J, Fu J & & Wang A 2015 Differential gene expression in uterine endometrium during implantation in pigs. Biology of Reproduction 92 52. (https://doi.org/10.1095/biolreprod.114.123075)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Choi I, Troyer DL, Cornwell DL, Kirby-Dobbels KR, Collante WR & & Simmen FA 1997 Closely related genes encode developmental and tissue isoforms of porcine cytochrome P450 aromatase. DNA and Cell Biology 16 769777. (https://doi.org/10.1089/dna.1997.16.769)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Conley A & & Hinshelwood M 2001 Mammalian aromatases. Reproduction 121 685695. (https://doi.org/10.1530/REP.0.1210685)

  • Conley AJ, Christenson RK, Ford SP, Geisert RD & & Mason JI 1992a Steroidogenic enzyme expression in porcine conceptuses during and after elongation. Endocrinology 131 896902. (https://doi.org/10.1210/ENDO.131.2.1379167)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Conley AJ, Graham-Lorence SE, Kagimoto M, Lorence MC, Murry BA, Oka K, Sanders D & & Mason JI 1992b Nucleotide sequence of a cDNA encoding porcine testis 17α-hydroxylase cytochrome P-450. Biochimica et Biophysica Acta 1130 7577. (https://doi.org/10.1016/0167-4781(9290464-B)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Conley AJ, Christenson LK, Ford SP & & Christenson RK 1994 Immunocytochemical localization of cytochromes P450 17 alpha-hydroxylase and aromatase in embryonic cell layers of elongating porcine blastocysts. Endocrinology 135 22482254. (https://doi.org/10.1210/ENDO.135.5.7956948)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Conley AJ, Corbin CJ, Hinshelwood MM, Liu Z, Simpson ER, Ford JJ & & Harada N 1996 Functional aromatase expression in porcine adrenal gland and testis. Biology of Reproduction 54 497505. (https://doi.org/10.1095/BIOLREPROD54.2.497)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Conley A, Corbin J, Smith T, Hinshelwood M, Liu Z & & Simpson E 1997 Porcine aromatases: studies on tissue-specific, functionally distinct isozymes from a single gene? Journal of Steroid Biochemistry and Molecular Biology 61 407413. (https://doi.org/10.1016/S0960-0760(9780040-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Corbin CJ, Berger T, Ford JJ, Roselli CE, Sienkiewicz W, Trainor BC, Roser JF, Vidal JD, Harada N & & Conley AJ 2009 Porcine hypothalamic aromatase cytochrome P450: isoform characterization, sex-dependent activity, regional expression, and regulation by enzyme inhibition in neonatal boars. Biology of Reproduction 81 388395. (https://doi.org/10.1095/biolreprod.109.076331)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Geisert RD, Whyte JJ, Meyer AE, Mathew DJ, Juárez MR, Lucy MC, Prather RS & & Spencer TE 2017 Rapid conceptus elongation in the pig: an interleukin 1 beta 2 and estrogen-regulated phenomenon. Molecular Reproduction and Development 84 760774. (https://doi.org/10.1002/MRD.22813)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Geisert RD, Johns DN, Pfeiffer CA, Sullivan RM, Lucas CG, Simintiras CA, Redel BK, Wells KD, Spencer TE & & Prather RS 2022 Gene editing provides a tool to investigate genes involved in reproduction of pigs. Molecular Reproduction and Development. (https://doi.org/10.1002/MRD.23620)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Golovine K, Schwerin M & & Vanselow J 2003 Three different promoters control expression of the aromatase cytochrome P450 gene (Cyp19) in mouse gonads and brain. Biology of Reproduction 68 978984. (https://doi.org/10.1095/BIOLREPROD.102.008037)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Graddy LG, Kowalski AA, Simmen FA, Davis SL, Baumgartner WW & & Simmen RC 2000 Multiple isoforms of porcine aromatase are encoded by three distinct genes. Journal of Steroid Biochemistry and Molecular Biology 73 4957. (https://doi.org/10.1016/s0960-0760(0000054-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Johns DN, Lucas CG, Pfeiffer CA, Chen PR, Meyer AE, Perry SD, Spate LD, Cecil RF, Fudge MA & Samuel MS et al.2021 Conceptus interferon gamma is essential for establishment of pregnancy in the pig†. Biology of Reproduction 105 15771590. (https://doi.org/10.1093/BIOLRE/IOAB186)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kaminski MA, Ford SP & & Conley AJ 1997 Differences in the expression of cytochromes P450 17α-hydroxylase and aromatase in Meishan and Yorkshire conceptuses at days 10.5–14.0 of gestation. Journal of Reproduction and Fertility 111 213219. (https://doi.org/10.1530/JRF.0.1110213)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kao YC, Higashiyama T, Sun X, Okubo T, Yarborough C, Choi I, Osawa Y, Simmen FA & & Chen S 2000 Catalytic differences between porcine blastocyst and placental aromatase isozymes. European Journal of Biochemistry 267 61346139. (https://doi.org/10.1046/j.1432-1327.2000.01705.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lee SH, Lee HS, Lim CK, Park YS, Yang KM & & Park DW 2013 Comparison of the clinical outcomes of day 4 and 5 embryo transfer cycles. Clinical and Experimental Reproductive Medicine 40 122125. (https://doi.org/10.5653/cerm.2013.40.3.122)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Meyer AE, Pfeiffer CA, Brooks KE, Spate LD, Benne JA, Cecil R, Samuel MS, Murphy CN, Behura S & Mclean MK et al.2019 New perspective on conceptus estrogens in maternal recognition and pregnancy establishment in the pig†. Biology of Reproduction 101 148161. (https://doi.org/10.1093/biolre/ioz058)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vanselow J, Conley AJ & & Berger T 2021a Aromatase and the three little paralogs. Biology of Reproduction 105 56. (https://doi.org/10.1093/biolre/ioab112)

  • Vanselow J, Conley AJ, Corbin CJ & & Berger T 2021b Genomic structure of the porcine CYP19 locus and expression of the CYP19A3 paralog. Genes (Basel) 12. (https://doi.org/10.3390/genes12040533)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Whyte JJ, Meyer AE, Spate LD, Benne JA, Cecil R, Samuel MS, Murphy CN, Prather RS & & Geisert RD 2017 Inactivation of porcine interleukin-1β results in failure of rapid conceptus elongation. Proceedings of the National Academy of Sciences of the United States of America 115 307312. (https://doi.org/10.1073/pnas.1718004115)

    • PubMed
    • Search Google Scholar
    • Export Citation